No full-text available
To read the full-text of this research,
you can request a copy directly from the authors.
Effects of deslorelin implants on reproduction and feeding behavior in Tasmanian devils ( Sarcophilus harrisii ) housed in free-range enclosures
Abstract
In captive breeding programs, it is becoming increasingly important to maximize the retention of genetic diversity by managing the reproductive contribution of each individual, which can be facilitated through the use of selective contraception. This becomes critical when captive populations are held for several generations, and managers must prevent the confines of housing space and financial support from compromising genetic integrity. For example, the Tasmanian devil insurance population, established in 2006, is strategically managed to equalize founder representation. This becomes difficult when devils are housed in large groups in free-range enclosures (FREs). This study examined the efficacy, duration and potential side effects of Suprelorin(®) contraceptive implants (containing 4.7 mg of deslorelin) on Tasmanian devils housed in FREs. Females were monitored to assess post-treatment reproductive rates, feeding behavior and weight changes. Suprelorin(®) successfully prevented reproduction in all treated females (P < 0.001) for at least one breeding season. For one year after contraception, there was no difference in proportion of time spent feeding between contraception and control groups (P > 0.05) and there was no effect of contraception on order of arrival at food (P = 0.632), suggesting no alterations to social structure. Devils with pouch young spent more time feeding than those without (P < 0.001). Treatment and month had an interactive effect on weight (P < 0.001), yet contracepted females were only heavier than controls in one season, indicating no overall excessive weight gain. Suprelorin(®) implants inhibit reproduction for at least one breeding season, with no apparent negative effects on feeding behavior or social dynamic. Selective contraception has the potential to become an important tool for conservation managers, to meet multiple reproductive, genetic and behavioral goals for this species.
... Knowledge of the duration of contraception is essential to ensure that the effects of a contraceptive are predictable in this endangered species. Since the commencement of this study, Suprelorin has been reported to successfully inhibit reproduction in female devils in free-range enclosures with no detectable negative effects (Cope et al. 2018a), but the duration of effect in females and efficacy in males has not been established. The present study provides the first detailed account of the physiological effects of these implants in both male and female devils, with detailed endocrine profiles during treatment and improved resolution of the duration of contraceptive effectiveness in females utilising different doses of Suprelorin. ...
... Veterinarians maintained and monitored animals under general anaesthesia with isoflurane during the GnRH challenge (see below), when a general health check was performed (BCS, blood analysis and physical examination) and the appearance of their pouch was observed and recorded. Pouches were given a score of 1-9 based on the STDP Standard Operating Procedure (1, immature; 2, pinkish, dry; 3, some oil, red; 4, lipstick ring, oil drops, puffy; 5-6, postovulatory; 7-9, pouch young or lactation); see fig. 1 in Cope et al. (2018a). Pouch appearance is a reliable reflection of the reproductive status of devils . ...
... Bodyweight is affected by prescribed diets aimed at maintaining an optimal body condition and these diet allocations are based on body condition, so the two variates are intermeshed and trends should not be assessed alone. Previous research on Tasmanian devils in free-ranging enclosures showed that there was no difference in overall weight between females on 4.7 mg Suprelorin implants (referred to as low dose in our study) and controls (Cope et al. 2018a). As such, if there is a treatment effect on weight, it may only be evident in intensively housed devils and in these situations it can be managed with changes to diet. ...
Contraception is increasingly used to manage breeding opportunities in conservation-dependent species. This study aimed to determine the efficacy, duration of effect, optimal dose and potential side effects of Suprelorin contraceptive implants in Tasmanian devils, for use in the conservation breeding program. In our pilot study, Suprelorin was found to effectively suppress oestrous cycles in female devils, yet caused a paradoxical increase in testosterone in males. Therefore, we focussed on females in further trials. Females received one (n = 5), two (n = 5) or no (n = 5) Suprelorin implants, with quarterly gonadotrophin-releasing hormone (GnRH) challenges used to test pituitary responsiveness over two breeding seasons. Both Suprelorin doses suppressed pituitary responsiveness for at least one breeding season, with a reduced effect in the second. There was a dose-response effect on duration rather than magnitude of effect, with high-dose devils remaining suppressed for longer than low-dose animals. There were no apparent negative effects on general health, yet captivity and contraception together may cause weight gain. Suprelorin contraceptive implants are now routinely used in the Save the Tasmanian Devil Program insurance metapopulation to meet the aims of maintaining genetic and behavioural integrity by controlling individual reproductive contributions in group housing situations.
... An additional 15 devils that were housed at the sites during this time could not be included, as no DNA sample was obtained, or the sample was of too poor quality to sequence. A further five females were contracepted during some of the enclosure years for a separate study (Cope et al., 2018), none of which produced offspring. Contracepted devils were excluded from all analyses. ...
Incorporating mate choice into conservation breeding programs can improve reproduction and the retention of natural behaviours. However, different types of genetic‐based mate choice can have varied consequences for genetic diversity management. As a result, it is important to examine mechanisms of mate choice in captivity to assess its costs and benefits. Most research in this area has focused on experimental pairing trials, however this resource‐intensive approach is not always feasible in captive settings and can interfere with other management constraints. We used generalised linear mixed models and permutation approaches to investigate overall breeding success in group‐housed Tasmanian devils at three non‐mutually exclusive mate choice hypotheses: (i) advantage of heterozygous individuals, (ii) advantage of dissimilar mates, and (iii) optimum genetic distance, using both 1,948 genome‐wide SNPs and 12 MHC‐linked microsatellites. The managed devil insurance population is the largest such breeding program in Australia and is known to have high variance in reproductive success. We found that non‐genetic factors such as age were the best predictors of breeding success in a competitive breeding scenario, with younger females and older males being more successful. We found no evidence of mate choice under the hypotheses tested. Mate choice varies among species and across environments, so we advocate for more studies in realistic captive management contexts as experimental or wild studies may not apply. Conservation managers must weigh up the need to wait for adequate sample sizes to detect mate choice with the risk that genetic changes may occur during this time in captivity. Our study shows that examining and integrating mate choice into the captive management of species housed in realistic, semi‐natural group‐based contexts may be more difficult than previously considered.
... An additional four adult females were housed in the enclosure but were contracepted as part of another study(Cope et al. 2018a) ...
Captive animals are commonly housed in groups to make efficient use of limited resources and allow for natural social behaviour. Captive management relies on accurate pedigrees to estimate various population genetic parameters, such as genetic contributions of breeders, but pedigrees of group-housed offspring can be uncertain. Pedigree analysis software incorporates genetic information from multiple putative parents (“MULT”). Molecular pedigree reconstruction to resolve pedigree uncertainties can be costly. We quantify the need for molecular parentage assignment by comparing predicted offspring contributions (based on uncertain “MULT” pedigrees) to contributions obtained from a molecular genetic pedigree reconstruction. Parentage of 81 insurance population Tasmanian devils (Sarcophilus harrisii) born in free-range enclosures from 2011 to 2017 was resolved using 891 single nucleotide polymorphisms. We observed large discrepancies between the MULT pedigree and molecular pedigree data, revealing both overestimates and underestimates of genetic contributions of individuals, and different pedigree-based effective population sizes (102 vs. 158 respectively). The molecular data revealed that reproductive skew (proportion of adults that failed to breed) was high for both sexes. Over half of the wild-born individuals in our dataset were found to have not bred. If undetected, variation in breeding success undermines the utility of pedigree management and may threaten the success of captive breeding. Molecular techniques are increasingly cost-effective, and our data demonstrate that they are critical to devil management. Where feasible, we recommend molecular management of group-housed species in captivity to avoid inaccurate estimates of genetic diversity and to identify non-breeding individuals, in particular founders, for targeted breeding.
Biodiversity conservation continually presents new challenges, yet conservation resources are limited, and funding for applied conservation research projects more so. Recently, many have reported on the "research-implementation gap," whereby conservation research findings are infrequently translated into conservation actions. In this perspective, we describe our experiences working in a large multi-institutional, multi-disciplinary team as we attempt to bridge the research-implementation gap by developing conservation tools needed to address the conservation challenges faced by Tasmanian devils (Sarcophilus harrisii). We discuss our project's history, lessons learnt, outcomes, and future plans to provide insights that may help others develop multi-institutional projects, designed to target rapid and direct implementation of conservation research into management action. Key to our success is the needs-based prioritization of research measured against the management team's questions, recognition of the different needs of academia, industry and government, a collegiate approach, and willingness to embrace adaptive management. Challenges include developing a project which meets all strategic targets of different institutions, in addition to sourcing funds. Overall, our goal has been to establish an enduring research-management framework, to facilitate improved integration of scientific research into the management needs of Tasmanian devil conservation, and serve as a template for other species management projects.
Life-history trade-offs between components of fitness arise because reproduction entails both gains and costs. Costs of reproduction can be divided into ecological and physiological costs. The latter have been rarely studied yet are probably a dominant component of the effect. A deeper understanding of life-history evolution will only come about once these physiological costs are better understood. Physiological costs may be direct or indirect. Direct costs include the energy and nutrient demands of the reproductive event, and the morphological changes that are necessary to facilitate achieving these demands. Indirect costs may be optional 'compensatory costs' whereby the animal chooses to reduce investment in some other aspect of its physiology to maximize the input of resource to reproduction. Such costs may be distinguished from consequential costs that are an inescapable consequence of the reproductive event. In small mammals, the direct costs of reproduction involve increased energy, protein and calcium demands during pregnancy, but most particularly during lactation. Organ remodelling is necessary to achieve the high demands of lactation and involves growth of the alimentary tract and associated organs such as the liver and pancreas. Compensatory indirect costs include reductions in thermogenesis, immune function and physical activity. Obligatory consequential costs include hyperthermia, bone loss, disruption of sleep patterns and oxidative stress. This is unlikely to be a complete list. Our knowledge of these physiological costs is currently at best described as rudimentary. For some, we do not even know whether they are compensatory or obligatory. For almost all of them, we have no idea of exact mechanisms or how these costs translate into fitness trade-offs.
An insurance population for the critically endangered Tasmanian devil was established in 2006. Due to successful captive breeding, the population has reached its carrying capacity of 600 devils and retains 99.95 % of founding gene diversity. Although reproduction has been quite successful, possible relatedness among founding individuals, influences of genetic provenance and pairing success on female productivity were evaluated to further refine insurance population management. Ten polymorphic microsatellite markers were used to assess the founders. Although the data were ultimately insufficient for determining specific founder relationships, a STRUCTURE analysis determined founders to be of eastern or western provenance. Western provenance animals had an observed heterozygosity of 0.38; while eastern provenance was 0.41. Allelic frequencies between the two provenances were similar. Although differences in pairing success of eastern and western provenance animals were noted, there was no difference in overall productivity (number of joeys/female). Cross-provenance pairings were not as successful as W–W but had similar productivity, and produced viable offspring. Birth origin (wild-born vs. zoo-born) had no influence on pairing success but wild-born females produce significantly more joeys/female. For zoo-born females, the number of joeys produced per female had a downward trend between respective generations in captivity. Current and future population managers should be aware of potential reductions in productivity across captive generations and adjust breeding recommendations accordingly. The ability to recruit founders from diseased females, along with a better understanding of the influence of genetic provenance and birth origin on productivity, has led to changes in acquisition of future founders for this insurance population.
Wildlife reintroductions and translocations are statistically unlikely to succeed. Nevertheless, they remain a critical part of conservation because they are the only way to actively restore a species into a habitat from which it has been extirpated. Past efforts to improve these practices have attributed the low success rate to failures in the biological knowledge (e.g., ignorance of social behavior, poor release site selection), or to the inherent challenges of reinstating a species into an area where threats have already driven it to local extinction. Such research presumes that the only way to improve reintroduction outcomes is through improved biological knowledge. This emphasis on biological solutions may have caused researchers to overlook the potential influence of other factors on reintroduction outcomes. I employed a grounded theory approach to study the leadership and management of a successful reintroduction program (the Sea Eagle Recovery Project in Scotland, UK) and identify four critical managerial elements that I theorize may have contributed to the successful outcome of this 50-year reintroduction. These elements are: 1. Leadership & Management: Small, dedicated team of accessible experts who provide strong political and scientific advocacy ("champions") for the project. 2. Hierarchy & Autonomy: Hierarchical management structure that nevertheless permits high individual autonomy. 3. Goals & Evaluation: Formalized goal-setting and regular, critical evaluation of the project's progress toward those goals. 4. Adaptive Public Relations: Adaptive outreach campaigns that are open, transparent, inclusive (esp. linguistically), and culturally relevant.
Context
Fertility control offers a non-lethal management technique for iconic yet overabundant wildlife. Slow-release hormonal implants containing deslorelin show promise for managing free-ranging populations, particularly in peri-urban reserves, but most studies have been limited to captivity.
Aims
We investigated the efficacy and mechanism of deslorelin implants in free-ranging female eastern grey kangaroos (Macropus giganteus) under realistic management conditions.
Methods
We assigned females to a deslorelin (9.4 mg, n = 53) or placebo (n = 56) group at three peri-urban sites in Victoria, Australia, and monitored reproductive success for 3 years by observing young in the pouch. We tested the plasma LH response of control and treated females to exogenous GnRH, and compared the size of ovarian follicles between the two groups.
Key results
Deslorelin implants reduced fertility at all three sites. No deslorelin-treated females bred in Year 1 at Anglesea and Serendip versus 42% and 44% of control females respectively. At Plenty Gorge, 60% of deslorelin-treated females bred in Year 1 versus 100% of control females. In Year 2, between 11% and 39% of the treated females bred versus between 82% and 100% of control females at all sites. The contraceptive efficacy reduced by Year 3 when between 43% and 57% of the treated females bred versus between 85% and 100% of controls. A GnRH challenge elicited higher plasma LH concentrations in control than in treated females, and unlike untreated females, treated females lacked ovarian follicles >2 mm.
Conclusions
Deslorelin implants reduced fertility in free-ranging female eastern grey kangaroos over three successive breeding seasons. Chronic exposure to deslorelin desensitised the pituitary gland to GnRH and suppressed follicular development, but did not inhibit the development of a blastocyst, pregnancy or lactation in at least some females that had conceived before treatment.
Implications
Effective population management using deslorelin implants will require females to be re-treated on multiple occasions because the contraceptive effect lasts only a portion of their reproductive life. This would be practical only at sites where kangaroos are relatively easy to capture. The timing of treatment is also important in a species that undergoes embryonic diapause, particularly at sites providing high-quality habitat.
Wildlife reintroduction programs are a type of conservation initiative that seek to re-establish viable populations of a species in areas from which they have been extirpated or become extinct. Past efforts to improve the outcomes of reintroduction have focused heavily on overcoming ecological challenges, with little attention paid to the potential influence of leadership, management, and other aspects of reintroduction. This 2009 survey of reintroduction practitioners identified several key areas of leadership and management that may deserve further study, including: (i) the potential value of reintroduction partnerships for improving programmatic outcomes; (ii) the potential management value of autonomy vs. hierarchy in organizational structure; (iii) gaps in perceptions of success in reintroduction; and (iv) the need for improved evaluations of reintroduction programs and outcomes.
The Tasmanian devil, Sarcophilus harrisii, the largest extant carnivorous marsupial, is normally solitary, but it congregates when feeding on carcasses. In this study, observations of behaviour during group feeding were used to document the communication and social organisation of these little-known animals. Their communication repertoire involved visual (20 postures), vocal (11 sound forms) and probably chemical signalling via urination and ano-genital drag. While some animals had conspicuous markings, 13% had none, suggesting that markings were not necessary for individual recognition. Agonistic interactions seldom resulted in physical clashes, but a few led to damage to the muzzle and rump, as supported by heavy scarring in these regions. Adult males were the most frequently and seriously scarred, probably related to agonistic encounters from longer feeding bouts and copulatory aggression. Devils gorged themselves, eating approximately 40% of their body mass. There was no apparent hierarchical structure to the sequence in which individuals fed. Feeding duration seemed to be determined by the extent to which an animal feeding on the carcass was sated.
In recent years fertility control has been proposed as an ethically acceptable alternative to lethal control techniques when managing overabundant kangaroo populations. A promising non-steroidal, non-immunological approach to contraception in female kangaroos involves the use of slow-release implants containing the gonadotrophin-releasing hormone (GnRH) agonist deslorelin. The practicality of using deslorelin implants as a management option is dependant on its effective inhibition of reproduction without negative physical or behavioural side-effects. This study investigated the behavioural effects of deslorelin implants in female eastern grey kangaroos. Treatment had no detectable effects on crepuscular activity. Alterations in the frequency of sexual interactions were observed in deslorelin-treated females, with a behavioural oestrus induced ~3 days after combined removal of pouch young and deslorelin administration. Copulation was observed during this early oestrous period, but conception was not achieved and pouch young were not observed in any treated females. Control females gave birth within 69.6 ± 10.4 days (mean ± s.e.m., n = 9) of placebo implant administration. The first births observed in treated animals were on Days 510, 637 and 643 after treatment. The remaining seven treated animals had not bred by the end of the study, a period of 647 days.
Two geographically separate populations of S. harrisii were studied. There is evidence that long-term population cycles exist in this species. Devils are non-territorial and have a home range which may be shared by several animals. Sclerophyll forest and coastal scrub are their favoured habitats. Individuals in the two populations showed different movements, probably related to food availability; those in areas of abundant food moved about 2 miles and had small home ranges whereas those in areas with less food moved over at least 10 miles per night. The density of population was high in one area, reaching over 30 per square mile, but this is abnormal. Devils have a wide food spectrum and use introduced species as well as native, but in each area their food was based upon one to three species. Man is the principal predator on adult devils. Females were more numerous in all populations but a heavier mortality of this sex occurs in late life. This differential mortality took place at immaturity in one population. Juvenile recruitment was greater in areas with less food than in areas of abundant food, due to the absence of overcrowding.
Eastern grey kangaroos are widespread on the east coast of Australia and frequently reach high densities in reserves and parkland near urban areas. Management of these populations is highly contentious and non-lethal fertility-control technologies are sought as an alternative option to manage population size. This study evaluated the potential of slow-release gonadotrophin-releasing hormone agonist (deslorelin) implants to inhibit reproduction in female kangaroos. Deslorelin treatment effectively inhibited reproduction in adult females for periods of 559 ± 111 days (n = 6) and 651 ± 21 days (n = 5) after administration of one or two 10-mg implants respectively. Animals treated with the lower dosage tended to resume breeding earlier than those that received a total of 20 mg of deslorelin (minimum duration of 18 months). Deslorelin treatment had no effect on blastocyst reactivation in a single treated female and repeat treatment had no negative side-effects. This study has demonstrated that slow-release deslorelin implants can successfully inhibit reproduction for extended periods in the female eastern grey kangaroos. This approach may have potential application in reproductive management of problem kangaroo populations.
When kangaroo populations reach high numbers in reserves and parkland near urban areas there are a number of implications. The animals may pose a risk to their own welfare as the population expands, have a negative effect on other aspects of the local biodiversity or impinge on human activities. In such cases active management of the population may be sought to ameliorate the negative effects. Traditional control techniques such as culling are often out of the question in these circumstances due to social pressures and concerns for human safety. In this paper I review three fertility control techniques that are potential management tools for these situations. Surgical sterilisation is a fertility control technique that has been used in a number of high profile situations. It is probably the most well established method of fertility control, is permanent, but is invasive and stressful. New biotechnological approaches to fertility control, such as the use of steroidal and non-steroidal contraceptives, are currently being trialled on kangaroos. These include the synthetic progestin levonorgestrel and the GnRH agonist deslorelin. These contraceptive agents are capable of successfully reducing the fertility of kangaroos for a range of durations depending on the agent used. Such contraceptive agents are likely to be a useful tool to manage both captive kangaroo populations and those in parkland areas. The development of a remote delivery technique will increase their efficacy for use in wild populations.
Lactation is the most energetically expensive component of reproduction in mammals. Theory predicts that reproducing females will adjust their behaviour to compensate for increased nutritional demands. However, experimental tests are required, since comparisons of the behaviour of naturally reproducing and non-reproducing females cannot distinguish between true costs of reproduction, individual differences or seasonal variation. We experimentally manipulated reproduction in free-ranging, eastern grey kangaroos (Macropus giganteus), using a fertility control agent. Our novel field experiment revealed that females altered their behaviour in direct response to the energetic demands of reproduction: reproducing females increased bite rates, and thus food intake, when the energetic demands of lactation were highest. Reproducing females did not reduce the time spent on vigilance for predators, but increased their forage intake on faecal-contaminated pasture, thereby increasing the risk of infection by gastrointestinal parasites-a largely unrecognized potential cost of reproduction.
The Tasmanian devil, Sarcophilus harrisii, is the largest extant marsupial carnivore. In 1996, a debilitating facial tumor was reported. It is now clear that this is an invariably lethal infectious cancer. The disease has now spread across the majority of the range of the species and is likely to occur across the entire range within 5 to 10 years. The disease has lead to continuing declines of up to 90% and virtual disappearance of older age classes. Mark-recapture analysis and a preliminary epidemiological model developed for the population with the best longitudinal data both project local extinction in that area over a timeframe of 10 to 15 years from disease emergence. However, the prediction of extinction from the model is sensitive to the estimate of the latent period, which is poorly known. As transmission appears to occur by biting, much of which happens during sexual encounters, the dynamics of the disease may be typical of sexually transmitted diseases. This means that transmission is likely to be frequency-dependent with no threshold density for disease maintenance. Extinction over the entire current range of the devil is therefore a real possibility and an unacceptable risk. Yes Yes
The high energetic costs of lactation can lead to fundamental trade-offs in life-history traits, particularly in young females that reproduce before completing body growth. We assessed whether lactating female mountain goats (Oreamnos americanus) used behavioural tactics at fine spatio-temporal scales to increase energy intake to compensate for the costs of lactation. Lactating females increased bite rate and chewing rate compared with non-lactating females, but selected similar foraging sites in terms of plant quality and abundance. At peak lactation, forage intake of lactating females was >40% greater than that of non-lactating females. For females that had reached asymptotic body mass (i.e. > or =6 years old), summer mass gain of lactating females was similar to that of non-lactating females. At 4 and 5 years of age, however, daily mass gain of lactating females was about 20% lower than that of non-lactating females. We conclude that increased foraging may allow fully-grown lactating females to compensate for the energetic costs of lactation, but that there is a major trade-off between mass gain and lactation for younger females.
The purpose of this article is to compare the energetics of reproduction for human and other primates in order to evaluate the extent to which human reproductive energetics are distinct from other primates and other large-bodied placental mammals. The article also evaluates the energetics of human and primate gestation and lactation using data from a variety of different populations living under different environmental circumstances. Energetics refers to energy intake and expenditure, and changes in body fat stores. Human and nonhuman primates have longer periods of gestation and lactation and slower prenatal and postnatal growth than other mammals of similar size. This reduces daily maternal energy costs. The development of sizable fat stores is not unique to humans, but fat stores are typically greater in human females and may play a greater role in reproduction. The strategies used to meet the energy costs of pregnancy vary among populations of humans and nonhuman primates and among humans interindividual variability is high. In pregnancy, some increase energy intake but others apparently do not. Increases in metabolic efficiency are evident in some human populations, whereas decreases in physical activity occur, but are not seen in all human or primate populations. Lactation is more energetically costly on a daily basis among humans and nonhuman primates, but has not been as well studied. It appears that both nonhuman and human primates tend to increase energy intake to meet in part the cost of lactation. They also use other strategies such as relying on body tissue stores, reductions in physical activity, and/or increases in metabolic efficiency to meet the remainder of the cost. It is also clear that human females in different populations and different women in the same population use a different combination of strategies to meet the cost of lactation.
Fertility control offers a potential alternative to traditional methods for regulating the growth of overabundant wild ungulate populations. However, current technology is limited due to practical treatment application, undesirable side-effects and economic considerations. A promising non-steroidal, non-immunological approach to contraception involves the use of a potent GnRH agonist. Two experiments were conducted to evaluate the effectiveness of a GnRH agonist (leuprolide) for controlling fertility in captive female wapiti and to assess physiological and behavioural side-effects of the treatment. In Expt 1, the optimum dose of agonist treatment was determined by measuring serum LH response of eight female wapiti to four formulations of leuprolide (0, 45, 90 and 180 mg) administered as a subcutaneous (s.c.) bioimplant. In Expt 2, the effects of leuprolide on wapiti pregnancy rates, duration of suppression of serum LH and progesterone secretion, and short-term behavioural and physiological side-effects were evaluated. All concentrations of leuprolide in Expt 1 were equally effective in reducing serum LH to non-detectable values throughout the 130 day trial. In Expt 2, leuprolide administered before the breeding season was 100% effective at preventing pregnancy in treated females. Serum LH and progesterone were reduced to baseline values by day 92 and remained at this concentration for 195-251 days after treatment, and returned to pretreatment concentrations in the following breeding season. Reproductive behaviour rates were similar for treated and untreated wapiti for all behaviour categories for both the breeding and post-breeding seasons. Haematology and blood chemistry parameters of treated and un-treated females were similar, and seasonal intake and body weight dynamics appeared normal. In conclusion, leuprolide is a safe, effective contraceptive agent and can potentially suppress fertility in female wapiti for one breeding season.
The contraceptive and endocrine effects of long-term treatment with implants containing the GnRH agonist deslorelin were investigated in female tammar wallabies (Macropus eugenii). Fertility was successfully inhibited for 515 +/- 87 days after treatment with a 5 mg deslorelin implant (n = 7), while control animals gave birth to their first young 159 +/- 47 days after placebo implant administration (n = 8). The duration of contraception was highly variable, ranging from 344 to 761 days. The strict reproductive seasonality in the tammar wallaby was maintained once the implant had expired. This inhibition of reproduction was associated with a significant reduction in basal LH concentrations and a cessation of oestrous cycles, as evidenced by low progesterone concentrations. There was evidence to suggest that some aspect of either blastocyst survival, luteal reactivation, pregnancy or birth may be affected by deslorelin treatment in some animals. These results show that long-term inhibition of fertility in the female tammar wallaby is possible using slow-release deslorelin implants. The effects of deslorelin treatment were fully reversible and there was no evidence of negative side effects. Slow-release GnRH agonist implants may represent a practicable method for reproductive management of captive and semi-wild populations of marsupials.
Life-history trade-offs between components of fitness arise because reproduction entails both gains and costs. Costs of reproduction can be divided into ecological and physiological costs. The latter have been rarely studied yet are probably a dominant component of the effect. A deeper understanding of life-history evolution will only come about once these physiological costs are better understood. Physiological costs may be direct or indirect. Direct costs include the energy and nutrient demands of the reproductive event, and the morphological changes that are necessary to facilitate achieving these demands. Indirect costs may be optional 'compensatory costs' whereby the animal chooses to reduce investment in some other aspect of its physiology to maximize the input of resource to reproduction. Such costs may be distinguished from consequential costs that are an inescapable consequence of the reproductive event. In small mammals, the direct costs of reproduction involve increased energy, protein and calcium demands during pregnancy, but most particularly during lactation. Organ remodelling is necessary to achieve the high demands of lactation and involves growth of the alimentary tract and associated organs such as the liver and pancreas. Compensatory indirect costs include reductions in thermogenesis, immune function and physical activity. Obligatory consequential costs include hyperthermia, bone loss, disruption of sleep patterns and oxidative stress. This is unlikely to be a complete list. Our knowledge of these physiological costs is currently at best described as rudimentary. For some, we do not even know whether they are compensatory or obligatory. For almost all of them, we have no idea of exact mechanisms or how these costs translate into fitness trade-offs.
The present study investigated the effects of slow-release implants containing the gonadotrophin-releasing hormone (GnRH) agonist deslorelin on reproduction in the common brushtail possum (Trichosurus vulpecula). Captive female brushtail possums were assigned to control (placebo implant), low dose (4.7 mg deslorelin) or high dose (9.4 mg deslorelin) groups; males were assigned to control or high dose (9.4 mg deslorelin) groups. The acute effects of deslorelin treatment at the level of the pituitary gland were similar between the two sexes, where a transient rise in luteinising hormone concentration was induced over the first 24 h. In females, this was associated with the disruption of the normal oestrous cycle and mating within 2–10 days in some treated individuals, but no young were subsequently detected. By 3 weeks after treatment, treated females became anoestrus and remained infertile for at least one breeding season. The effects of treatment were reversible in a subset of females that had their implants removed, although the time taken to produce offspring was variable. Paradoxically, male brushtail possums remained fertile during chronic deslorelin exposure. Despite significant declines in basal follicle-stimulating hormone and testosterone concentrations, as well as an inability to respond to a GnRH challenge, treated males sired as many offspring as control males and there was no evidence of testicular regression. In conclusion, there is potential to control reproduction in female brushtail possums by using chronic GnRH agonist treatment.
en Contraception has an established role in managing overabundant populations and preventing undesirable breeding in zoos. We propose that it can also be used strategically and selectively in conservation to increase the genetic and behavioral quality of the animals. In captive breeding programs, it is becoming increasingly important to maximize the retention of genetic diversity by managing the reproductive contribution of each individual and preventing genetically suboptimal breeding through the use of selective contraception. Reproductive suppression of selected individuals in conservation programs has further benefits of allowing animals to be housed as a group in extensive enclosures without interfering with breeding recommendations, which reduces adaptation to captivity and facilitates the expression of wild behaviors and social structures. Before selective contraception can be incorporated into a breeding program, the most suitable method of fertility control must be selected, and this can be influenced by factors such as species life history, age, ease of treatment, potential for reversibility, and desired management outcome for the individual or population. Contraception should then be implemented in the population following a step‐by‐step process. In this way, it can provide crucial, flexible control over breeding to promote the physical and genetic health and sustainability of a conservation dependent species held in captivity. For Tasmanian devils (Sarcophilus harrisii), black‐flanked rock wallabies (Petrogale lateralis), and burrowing bettongs (Bettongia lesueur), contraception can benefit their conservation by maximizing genetic diversity and behavioral integrity in the captive breeding program, or, in the case of the wallabies and bettongs, by reducing populations to a sustainable size when they become locally overabundant. In these examples, contraceptive duration relative to reproductive life, reversibility, and predictability of the contraceptive agent being used are important to ensure the potential for individuals to reproduce following cessation of contraception, as exemplified by the wallabies when their population crashed and needed females to resume breeding.
Abstract
es Un Papel en la Conservación para la Anticoncepción Selectiva de Individuos
Resumen
La anticoncepción tiene un papel establecido en el manejo de poblaciones sobreabundantes y en la prevención de reproducción indeseada en los zoológicos. Proponemos que también puede usarse estratégica y selectivamente en la conservación para incrementar la calidad genética y de comportamiento de los animales. En los programas de reproducción en cautiverio es cada vez más importante maximizar la retención de la diversidad genética manejando la contribución reproductiva de cada individuo y previniendo la reproducción subóptima genéticamente por medio del uso de la anticoncepción selectiva. La represión reproductiva de individuos selectos en los programas de conservación tiene más beneficios, como permitir a los animales ser alojados en grupo en recintos extensos sin interferir con las recomendaciones reproductivas, lo que reduce la adaptación al cautiverio y facilita la expresión de comportamientos y estructuras sociales de vida libre. Antes de que la anticoncepción selectiva pueda ser incorporada a un programa de reproducción, se debe elegir el método de control de la fertilidad más adecuado, y esto puede estar influenciado por factores como la historia de vida de la especie, la edad, la facilidad de manejo, el potencial para la reversibilidad, y el resultado deseado de manejo para el individuo o la población. Después de esto se debe implementar la anticoncepción dentro de la población siguiendo un proceso de paso‐por‐paso. De esta manera, puede proporcionar un control decisivo y flexible sobre la reproducción para promover la salud física y genética y la sustentabilidad de una especie dependiente de la conservación que se encuentra en cautiverio. Para los demonios de Tasmania (Sarcophilus harrisii), los walabíes de las rocas de flancos negros (Petrogale lateralis), y las ratas canguro de nariz corta (Bettongia lesueur), la anticoncepción puede beneficiar su conservación al maximizar la diversidad genética y la integridad conductual en el programa de reproducción en cautiverio, o, en el caso de los walabíes y las ratas canguro, al reducir a las poblaciones a un tamaño sustentable cuando se vuelvan sobreabundantes localmente. En estos ejemplos, la duración de la anticoncepción en relación a la vida reproductiva, la reversibilidad, y la predictibilidad del agente anticonceptivo que se usa son importantes para asegurar el potencial de reproducción de los individuos una vez que cese la anticoncepción, como se ejemplifica con los walabíes cuando su población colapsó y necesitó de hembras para reanudar su reproducción.
摘要
zh 节育是动物园管理数量过多动物种群数量和避免不恰当繁殖的一项措施。我们认为节育也可以战略性和选择性地用于动物保护, 以提高动物遗传和行为的质量。在圈养繁育项目中, 通过控制每个个体参与繁殖来保留最高的遗传多样性, 并通过选择性节育防止非最优的繁殖已变得越来越重要。保护项目中选择性地抑制个体繁殖有利于动物在大围栏内集群生活, 而不会破坏繁育计划, 这不仅能减少了动物对圈养环境的适应, 而且能促进它们展现野生生活的行为和社会结构。在将选择性节育纳入繁育项目之前, 我们应选出最适合的节育方法, 而这会受到物种的生活史、年龄、处理难度及可逆性潜力和对个体或种群预期的管理结果等因素的影响。接下来, 节育应在种群中逐步推行。这样可以有效且灵活地控制动物的繁殖, 以提高依赖于圈养保护物种的身体健康、遗传健康和可持续性。对于袋獾 (Sarcophilus harrisii) 、黑胁小岩袋鼠 (Petrogale lateralis) 和穴居草原袋鼠 (Bettongia lesueur), 节育可以最大化它们在圈养繁育项目中的遗传多样性和行为完整性, 而对于小袋鼠和草原袋鼠, 节育使局部地区数量过多的种群减少到可持续的数量, 有利于物种的保护。在这些例子中, 要确保个体在节育终止后可以繁殖, 节育持续的时间相对于繁殖年限、可逆性和采取节育方式的可预见性非常重要, 这一点在小袋鼠种群崩溃、需要雌性来重新恢复繁殖时有所体现。翻译: 胡怡思; 审校: 魏辅文
There has been much discussion relating to the current biodiversity crisis, with the loss of species now at an unprecedented rate. Using augmentation and/or reintroduction to minimize the loss of species in the wild is becoming more prominent. Zoological institutions have been traditionally involved in the management of insurance populations providing a range of species for release to the wild. Insurance populations can be costly, both in resources and behavioural changes, and so should aim to be maintained for as short a time as possible, with a maximum of 40 years. A Tasmanian devil Sarcophilus harrisii insurance population was established in 2006 with the arrival of devil facial tumour disease, and was founded with 120 individuals sourced predominantly from the west coast of Tasmania. Here the challenges of establishing and managing an insurance population in an already genetically depauperate species in the presence of a contagious cancer are discussed. The Tasmanian devil insurance metapopulation now includes a continuum of management scenarios (from intensive zoo-based facilities, through free-range enclosures, to an island and fenced peninsula) and consists of over 700 devils representing at least 180 founders. The lessons learned in regard to this programme are presented, including the issues surrounding reduced genetic diversity and how we are striving to improve the long-term management of the insurance metapopulation through a combination of molecular genetics, modelling and on-the-ground management. The tools and technologies that have been developed in this programme are directly applicable to the recovery and management of a suite of other threatened fauna.
The Tasmanian devil, Sarcophilus harrisii (Boitard), is the largest of living dasyurid marsupials, except for the doubtfully extant thylacine or Tasmanian tiger, Thylacinus cynocephalus. Recent ecological studies have investigated its numbers, diet and economic importance (Green, 1967; Guiler 1970a, b and c), and some aspects of its behaviour have also been reported. Early accounts (for example, Le Souef and Burrell, 1926) gave some details of agonistic behaviour, vocalisations and maintenance activities, which have been augmented in more recent reviews of marsupial biology (Walker, 1964; Troughton, 1965; Ride, 1970). Fleay (1935, 1952) described methods of fighting, grooming and comfort behaviour, resting, feeding, drinking, and changes in behaviour associated with individual development, and Guiler (1964, 1971) and Green (1967) gave further details of maintenance activities and social behaviour. Other studies by Ewer (1969) and Moeller (1972a, b, c; 1974) focused exclusively on prey-killing and feeding behaviour of the species. The Tasmanian devil is of considerable interest as a carnivorous marsupial successfully adapting to a changing environment. Field studies are difficult because of their mainly nocturnal activities, dark colour, cryptic habits and timidity towards man. The present study is based mainly on captive devils observed over several years at the University of Tasmania, and forms part of a series of continuing projects on selected problems of dasyurid behaviour. Our conclusions on prey-killing and feeding, agonistic interactions and social communication, and cloacal dragging, are drawn mainly from quantitative records; full reports will be published elsewhere.
Zoos and other ex situ wildlife institutions can play an important role in species conservation by maintaining populations for education and research, as sources for potential re-introduction or reinforcement, and as ambassadors for financial support of in situ conservation. However, many regional zoo associations are realizing that current captive populations are unsustainable, with many programs failing to meet demographic and genetic goals to ensure long-term viability. Constraints on population size due to limited space often mandate delayed and/or less frequent breeding, but for females of many species this can have profound effects on fertility. A retrospective analysis combined with published literature and reliable anecdotal reports reveals that, when females are housed in a non-breeding situation for extended periods of time, reproductive changes that negatively impact fertility have occurred in multiple species, including canids, elephants, white rhinoceros, Seba's bats, wildebeest, stingrays, and some felid species. Competing space needs and changing interest in taxa for exhibits over time compound the problem. Counter strategies to breed early and often have their own demographic and genetic consequences as well as logistical and political implications. Strategies to mitigate the sustainability crisis in these taxa might include a mixed strategy in which young, genetically valuable females are bred earlier and at more regular intervals to ensure reproductive success, in combination with the judicious use of available tools to manage the number of offspring produced, including contraception and culling. An understanding of the issues at stake is the first step towards developing management strategies for sustainable populations. Zoo Biol. 9999:1-9, 2013. © 2013 Wiley Periodicals, Inc.
The Tasmanian devil, S. harrisii, is polyovular and monoestrus and embryonic
diapause was not found. The mean number of pouch young for 69 litters was found
to be 2.95. The number of young in a litter varies with the age of the mother. More
young are born than can be accommodated in the pouch.
The time of breeding varies from year to year, mating taking place in March.
The percentage of breeding females varies annually as well as from place to place,
being found to be as low as 31 % in one area. The devil has a high reproductive
potential because there are no losses at the pouch-young stage. This is offset by poor
recruitment of juveniles into the population.
Pseudopregnancy was found to occur.
The sex ratio of both pouch young and adults favoured the female. The development and growth of the young is described.
Food intake and digestion were investigated at four stages in the first 218 days of lactation in tammar wallabies (Macropus eugenii) carrying litters of one, and in non-lactating females as a control. This period of lactation in tammars, which includes the phase of exponential growth of the young, is comparable to gestation plus early lactation in ruminant placentals. Food and energy intakes by mothers remained at the non-lactating level while rate of growth of young was slow (up to Day 105 of lactation) but then rose as the growth rate of young increased, keeping pace with the predicted requirements for milk synthesis and export. There was no indication of the energy deficit seen in late gestation and early lactation in many herbivorous placental mammals. The gross efficiency of utilization of ME for growth of offspring was estimated as 13–15%, which is at least as high as values for placentals during gestation. The mean intake of metabolizable energy (ME) at 218 days was 603 kJ.kg-0.75.d-1, which represented 136% of ME intake by nonlactating females, or an increment of 159 kJ.kg-0.75.d-1. It was estimated that ME intake may rise to 773 kJ.kg-0.75.d-1 at peak lactation, which would be 174% of the non-lactating level or an increment of 329 kJ.kg-0.75. d-1. This allometrically-scaled increment is similar to values for some ruminants that use body reserves extensively to offset peak lactational food requirements. These and previously-reported trends suggest that ecologically comparable herbivorous marsupials and placentals utilize different physiological strategies to minimize demands on food resources during reproduction, but that both daily and overall demands can be similar.
Female Tasmanian devils (TDs) Sarcophilus harrisii and spotted-tailed quolls (STQs) Dasyurus maculatus were monitored to assess changes in plasma progesterone and faecal oestrogens/progestagens, vaginal smears and qualitative changes in pouch appearance during the oestrous cycle. Pouch condition was characterized based on size, colour and secretions, and was found to accurately reflect reproductive status, being significantly correlated with changes in both sex steroids and vaginal cytology. During the follicular phase, pouch redness and secretions were maximal, and associated with increased sex steroid concentrations, a karyopyknotic index of >90% and the onset of copulation. Post-ovulation, pouches became wet and deep and developed a glandular appearance; plasma progesterone/faecal progestagen concentrations remained high and sustained throughout the luteal phase. These features were identical during the pregnant and non-pregnant oestrous cycle. This study demonstrated that pouch appearance is a reliable physical indicator of the stage of oestrous in the TD and STQ, and provides an alternative non-invasive method for evaluating the ovarian cycle of these threatened species. This technique can be readily applied to monitor individuals in free-ranging or captive populations, and will aid as a practical tool for improved breeding management.
The interaction patterns of two pairs of the Tasmanian Devil, Sarcophilus harrisii, were studied. We formulated a description for the major postures and configurations involved in agonistic, contact promoting, and sexual behavior. Vocalizations were analyzed and a syntactic classification of syllable types was formulated. The vocalizations recorded from intraspecific encounters run with pairs of marsupials from ten species were analyzed and compared with the syllable types so defined for Sarcophilus. Marsupial vocalizations were then compared with the vocalization patterns described for viverrid carnivores.
The ability of gonadotrophin releasing hormone (GnRH) agonist implants to suppress ovarian activity and prevent pregnancies, long-term, was examined in heifers and cows maintained under extensive management. At three cattle stations, heifers (2-year-old) and older cows (3- to 16-year-old) were assigned to a control group that received no treatment, or were treated with high-dose (12 mg, Station A) or low-dose (8 mg, Station B and Station C) GnRH agonist implants. The respective numbers of control and GnRH agonist-treated animals (heifers + cows) at each station were: Station A, 20 and 99; Station B, 19 and 89; Station C, 20 and 76. Animals were maintained with 4% bulls and monitored for pregnancy at 2-monthly intervals for approximately 12 months. Pregnancy rates for control heifers and control cows ranged from 60-90% and 80-100%, respectively, depending on the study site. The respective number of animals (heifers + cows) treated with GnRH agonist that conceived, and days to first conception, were: Station A, 9 (9%) and 336 +/- 3 days; Station B, 8 (10%) and 244 +/- 13 days; Station C, 20 (26%) and 231 +/- 3 days. Treatment with high-dose GnRH agonist prevented pregnancies for longer (approximately 300 days) than treatment with low-dose GnRH agonist (approximately 200 days). In the majority of heifers and cows treated with GnRH agonist, ovarian follicular growth was restricted to early antral follicles (2-4mm). The findings indicate that GnRH agonist implants have considerable potential as a practical technology to suppress ovarian activity and control reproduction in female cattle maintained in extensive rangelands environments. The technology also has broader applications in diverse cattle production systems.
Koalas are generally considered to be limited by their ability to acquire energy from their diet of Eucalyptus foliage and have the lowest mass-specific peak lactational energy output measured in any mammal to date. This study considered the energetics and sources of energy utilised for reproduction in free-ranging female koalas. Energy requirements and foliage intake were greater in both lactating and non-lactating females in winter than summer, presumably due to demands of thermoregulation. Koalas met the peak energy requirements of lactation primarily by a 36% increase in their intake of foliage. Metabolic energy expenditure (field metabolic rate, 1778 kJ.day(-1) for a 6.25-kg female at the time of peak lactation) was not elevated during lactation. This was due to compensation for part of their lactational demands by reduction of another, non-reproductive, component of their energy budget. The observed energetic compensation was probably due primarily to substitution of the waste heat from the metabolic costs of milk production and increased heat increment of feeding for thermoregulatory energy expenditure. There may also have been energetic compensation by reduction of some aspect of maintenance metabolism. Such energetic compensation, together with the strategy of spreading lactation over a long period, minimises the magnitude of lactational energy demands on koalas, and thus the increase in daily food intake required during lactation. As the nutritional requirements of females at peak lactation are the highest of any members of the population, low reproductive requirements effectively increase the types and amount of habitat able to support koala populations.
Wildlife contraception: issues, methods, and application
- C S Asa
Asa CS. Assessing efficacy and reversibility. In: Asa CS, Porton IJ, editors.
Wildlife contraception: issues, methods, and application. Baltimore, Maryland: The John Hopkins University Press; 2005. p. 53e65.
Captive management plan: tasmanian devil conservation program. Zoo and Aquarium Association
- C Hogg
- D Lee
Hogg C, Lee D. Captive management plan: tasmanian devil conservation
program. Zoo and Aquarium Association; 2014. p. 1e28.
Annual report and recommendations for the DPIPWE-ZAA tasmanian devil insurance population
- C J Hogg
- C Srb
Hogg CJ, Srb C. Annual report and recommendations for the DPIPWE-ZAA
tasmanian devil insurance population. Sydney, Australia: Zoo and Aquarium
Association; 2016. p. 1e22.
Climate data online. Australia: Australian Government
- Meterology Bureau Of
Bureau of Meterology. Climate data online. Australia: Australian Government;
2017.
Social organisation and behaviour of the Tasmanian devil, Sarcophilus harrisii
- D Pemberton
Pemberton D. Social organisation and behaviour of the Tasmanian devil,
Sarcophilus harrisii. University of Tasmania; 1990.
AZA reproductive management centre
- Aza Rmc
AZA RMC. In: Asa C, editor. AZA reproductive management centre. St. Louis,
MO: Saint Louis Zoo; 2016.
Tasmanian devil: a unique and threatened animal
- D Owen
- D Pemberton
Owen D, Pemberton D. Tasmanian devil: a unique and threatened animal.
Crows Nest, N.S.W. Allen & Unwin; 2005.