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Retrospective characterization of reproductive tract lesions in relation to age, parity, and contraception in captive suidae and tayassuidae
Abstract
Reproductive management in zoos requires contraception or physical separation of sexes to ensure captive population viability, but information is sparse on the effects of parity, age, and contraceptive use on lifetime reproductive health in captive Suidae and Tayassuidae species. This retrospective study evaluated reproductive tissues and histories from babirusa (Babyrousa babyrussa), red river hog (Potamochoerus porcus), Visayan warty pig (Sus cebifrons), common warthog (Phacochoerus africanus), Vietnamese pot-bellied pig (Sus scrofa domesticus), domestic cross pig (Sus scrofa), Sunda island pig (Sus celebensis timoriensis), Eurasian boar (Sus scrofa), Bornean bearded pig (Sus barbatus), Ossabaw island hog (Sus scrofa domesticus), Guinea hog (Sus scrofa domesticus), Chacoan peccary (Catagonus wagneri), and collared peccary (Pecari tajacu). Age, parity, litter size, time-since-last-parturition, contraception exposure and type, and lesion prevalence were recorded. Reported chemical contraceptives used in females included porcine zona pellucida vaccine, progestins, GnRH analogues (deslorelin and leuprolide). Average litter size was significantly different between species (p < 0.0001) with the common warthog having the largest average litter size (3.5 ± 0.2 offspring/litter). There was a trend for age to be positively correlated with leiomyoma/sarcomas (r = 0.6135; p = 0.0789). Progestins (medroxyprogesterone acetate, megestrol acetate, depomedroxyprogesterone acetate) were positively correlated (r = 0.8946; p = 0.0161) and GnRH analogues (deslorelin, leuprolide; subcutaneous) were negatively correlated with ovarian cysts (r = 0.9743; p = 0.0010). Across all species, there was a trend for age to be negatively correlated with folliculogenesis (r = −0.6528; p = 0.0566) and parturition gap length to be negatively correlated with follicular cysts (r = −0.8944; p = 0.1). Common warthog, babirusa, and Vietnamese pot-bellied pigs had the greatest diversity of uterine lesions and the highest prevalence of reproductive tract lesions of all species evaluated. Four of the 27 males (14.5%) in the dataset had testicular tumors. All males had prominent testicular interstitial cell populations, which appears to be within normal limits for these species. These data suggest prolonged gaps between pregnancies, age, and contraception are risk factors for reproductive tract lesions in Suidae.
... Notably, although captive wildlife are often administered contraceptive treatment, which has been associated with non-neoplastic genital tract lesions and some reproductive neoplasms, no association has been found between contraceptive exposure and uterine smooth muscle tumor development. 3,7 There was no history of contraceptive administration to the female capybara in this collection. Age is well-recognized as a risk factor for uterine smooth muscle neoplasms in various species. ...
... Age is well-recognized as a risk factor for uterine smooth muscle neoplasms in various species. 7,20 Given that the typical lifespan of a capybara is 8-10 y, 9 the advanced age of this animal was likely the primary predisposing factor. ...
A 10.5-y-old intact female capybara ( Hydrochoerus hydrochaeris) with a history of chronic weight loss was euthanized following discovery by palpation of a large intra-abdominal mass. Postmortem examination revealed a large, firm, tan mass expanding the uterine body and extensively adhered to the jejunum and abdominal wall. Numerous pinpoint to 3-cm diameter, tan-to-red, raised masses were present throughout the parietal peritoneum, liver, lungs, and intestinal serosa. Histologic examination of the uterine mass revealed well-differentiated smooth muscle intermixed with abundant collagen, interspersed with a highly anaplastic spindle cell population extending to the serosa; the masses in the lung, liver, and peritoneum were histologically very similar to the anaplastic uterine spindle cells. Immunohistochemical staining of the uterus and lung confirmed smooth muscle origin of the anaplastic cells. To our knowledge, leiomyosarcoma has not been reported previously in a capybara, and the widespread metastases in this case represent an unusually aggressive presentation of this rare malignancy. The animal also had an incidental dermal histiocytoma, a tumor that has also not been reported previously in this species, to our knowledge.
... Two histopathological lesions, potentially attributable to extended levels of progestogens, were identified, ovarian cysts and mild uterine endometrial hyperplasia. In suids and tayasuids, use of progesterone-based contraception is associated with increased risk of ovarian cysts (Goblet 2019). Moreover, synthetic progestogen use is a risk factor for endometrial hyperplasia, hydrometra, fibrosis and adenomyosis (Moresco 2009) and pyometra (Asa 2014) in canids, whilst in felids, it has been associated with malignant mammary neoplasia (McAloose 2007). ...
Rodrigues fruit bats Pteropus rodricensis breed well in captivity and require active population management. Halved etonogestrel implants (34 mg dose) were implanted in 138 female bats either subcutaneously in the brachium, or dorsum, and proved 100% efficacious in both locations. Duration of action was up to 36 months. Implant losses varied by location with 34.8% loss over four years from the brachial site, but only 1.3% loss over two years at the dorsal site. Of bats which lost their implants, 34.5% were found to be pregnant at replacement, indicating reversal is possible. Possible side effects were significant weight gain one year after contraception (mean gain 21.4%) and two possible sequelae to progesterone-based contraception were noted at post-mortem examination of implanted bats that died during the programme; ovarian cysts and mild cystic endometrial hyperplasia. Further data are needed to establish if there is a link to the use of etonogestrel as insufficient pre-contraception data were available. Aglepristone (4.5 mg dose, subcutaneously, twice 24 hours apart) was 75% effective at terminating early pregnancies (<10 mm diameter). Aglepristone failure (confirmed pregnancies that did not terminate with aglepristone) increased as female age increased (odds ratio (OR) 1.7; P=0.02) and there was a tendency for aglepristone failure to decrease with increased pregnancy size (mm), but this was not significant (OR=1.7; P=0.07). No side effects attributable to aglepristone were noted. Breeding was successfully controlled in a population of 239 bats to reduce the colony size over time. At present growth and mortality rates, with 85-90% of females contracepted and a birth rate per sexually mature female of ~0.13/year, compared to an average of 1.08/year prior to the programme, the colony can be managed down to <175 bats over the next 5-6 years. Etonogestrel implants and aglepristone can be successfully used as part of a population management strategy in Rodrigues fruit bats.
... It was postulated that long-term, lifetime exposure to estradiol and progesterone through many estrous cycles may contribute to carcinogenesis in suid species, as is recognized in women. 19 Among other exotic ungulates, rhinoceroses are notable for a high prevalence of reproductive tract leiomyomas, and similar to elephants, represent another charismatic megavertebrate for which reproduction in the managed care setting is a conservation goal. 15,24,26,55 In Indian rhinoceros (Rhinoceros unicornis) particularly, age-related development of reproductive tract leiomyomas has been implicated in reduced fecundity of the species in managed care. ...
Recent reports have highlighted a lower-than-expected prevalence of neoplasia in elephants and suggested mechanisms for cancer resistance. But despite infrequent reports in the literature, uterine neoplasia is common in managed Asian elephants (Elephas maximus). This study is an archival review of reproductive tract neoplasia in 80 adult female Asian elephant mortalities in managed care facilities in the United States from 1988 to 2019. Neoplasms occurred in 64/80 (80%) of cases. Most were in the uterus (63/ 64; 98%) with only a single case of ovarian neoplasia. Myometrial leiomyomas were present in 57/63 (90%) cases with uterine neoplasia. Uterine adenocarcinoma was present in 8/63 (13%) cases. Remaining cases included endometrial adenoma (2), focal carcinoma in situ in endometrial polyps (1), anaplastic carcinoma (1), endometrial hemangioma (1), primitive neuroectodermal tumor (PNET; 1), and angiosarcoma (1). One case with uterine adenocarcinoma had a separate pelvic mass histologically characterized as an anaplastic sarcoma. Distant metastases were documented in 5/8 (63%) cases of uterine adenocarcinoma, and in the uterine anaplastic carcinoma, PNET, and angiosarcoma. Four uterine adenocarcinomas and one carcinoma in situ were examined immunohistochemically for pan-cytokeratin, vimentin, and estrogen receptor. In all, neoplastic cells were pan-cytokeratin positive and vimentin negative, and in 2 cases were immunoreactive for estrogen receptor. Results show that female reproductive tract neoplasia, particularly of the uterus, is common in Asian elephants and is not limited to leiomyomas. Importantly, uterine neo-plasms have the potential to impact fecundity and may represent obstacles to conservation in managed care.
... In some taxa, the use of MGA implants (and other progestins) is associated with other adverse effects. The long-term use of progestins is associated with uterine and mammary cancer in felids (Munson & Moresco, 2007;Munson et al., 2002;Munson, 2006), endometrial hyperplasia and pyometra in felids and canids Moresco et al., 2009), and an increase in ovarian cysts in suids (Goblet et al., 2019). Whereas these issues have not been reported in primates, weight gain is commonly associated with progestin use in primates as well as other taxa (Möhle et al., 1999;Portugal & Asa, 1995;Wallace et al., 2016). ...
Melengestrol acetate (MGA) implants are progestin‐based reversible contraceptives used to manage fertility in zoo populations. Although it is recommended that MGA implants should be replaced every 2 years, the duration of efficacy has not been systematically evaluated in most species. Anecdotal reports for Old World monkeys indicate that reproduction may be suppressed longer if the implant is not removed. This study uses Guereza colobus monkey (Colobus guereza) as a model Old World monkey species to examine the effects of MGA implants on reproductive potential. In particular, we investigate whether the probability of reproducing (pR) and rates of stillbirth differ among (1) non‐implanted females, (2) females who have had MGA implants removed, and (3) females whose implants were left in past expiration. We found no significant difference in pR between non‐implanted and implant‐removed groups, but when implants were left in past expiration, the pR was significantly lower than in other groups. Both parity and age significantly impacted pR for the non‐implanted group (i.e., younger females and those who were parous increased pR), but neither were significant factors for the implant‐removed group. Stillbirth rates were significantly higher post‐contraception as compared with pre‐contraception. These results support similar analyses in other taxa that show a shorter time to reversal after MGA contraception when implants are removed, making this a good contraceptive option for females likely to receive a breeding recommendation, especially when a more predictable time to reversal is important.
Research Highlights
• Melengestrol acetate (MGA) implants are a good contraception option for females likely to receive a future breeding recommendation.
• Future probability of reproducing was higher if implants were removed.
• Stillbirth rates were higher after MGA implant contraception.
Reproductive tumors can impact conception, pregnancy, and birth in mammals. These
impacts are well documented in humans, while data in other mammals are limited. An urgent need exists to understand the reproductive impact of these lesions in endangered species, because some endangered species have a documented high prevalence of reproductive tumors. This article documents that the prevalence of both benign and malignant neoplasia differs between African and Asian elephants, with Asian elephants more frequently diagnosed and negatively affected by both.
The prevalence of these tumors across mammalian species is compared, and impact plus treatment options in human medicine are reviewed to inform decision making in elephants. Evidence suggests that reproductive tumors can negatively impact elephant conservation. Future studies that document reproductive outcomes, including the success of various treatment approaches in elephants with tumors will benefit conservation efforts.
Wildlife conservation requires varying degrees of management of endangered species as well as management of their potential predators and competitors. Conservation also depends on ameliorating human-wildlife conflict, especially where there is a threat to the safety of people and of their pets and livestock. In addition, sustainability of wildlife populations can be affected by feral domestic animals or invasive species, that require removal or control. With the increasing concern for animal welfare, non-lethal methods of limiting population size and distribution, such as fertility control, are gaining favor. Breeding programs in zoos depend on highly effective and selective contraception to manage sustainable insurance populations. This review covers fertility control methods currently in use, those that have not lived up to past promises, and others that are under development and present hope for addressing remaining challenges.
Subsistence hunting practiced by poor rural and indigenous people in Latin America differentially affects the three species of peccaries (Artiodactyla: Tayassuidae). Sustainability of subsistence hunting of peccaries in the Argentine semi-arid Chaco, where the three species coexist, was unknown. My objectives were to determine the importance of peccaries for the local people, describe the current pattern of hunting and its impact on the three species of peccary and identify the factors that affect hunting sustainability. I found that many rural (70%) and village people (40%) consumed peccaries. White-lipped and chacoan peccaries were more susceptible to overharvesting than collared peccary. Current rates of hunting of white-lipped and chacoan peccaries are likely not sustainable because: (a) density of both species was between two to three times higher inside a protected area than outside; (b) populations have declined near larger villages and in older settlements; (c) herds sizes were small in comparison with other regions; (d) large number of juveniles less than one year old were harvested; (e) hunting did not discriminate based on sex or reproductive status and (f) The unified harvest model indicated unsustainable harvest because more than 40% of the reproductive production was taken and populations densities were less than 60% carrying capacities. In contrast, harvest of collared peccary seems sustainable at the current rates of hunting by rural peasants. Other threats such as forest exploitation, however, are accelerating, and are likely to reduce sustainability.
the method of treatment used in the other groups immediately after the diagnosis was intramuscular administra - tion of lecirelin in doses 50 µg (Group 2, n = 28), 100 µg (Group 3, n = 27) and 200 µg divided into 2 equal doses administered at a 12-hour interval (Group 4, n = 25) and of hCG in doses 1 500 IU (Group 5, n = 23), 3 000 IU (Group 6, n = 21), and 250 µg of cloprostenol (Group 7, n = 24). Insemination rate (IR), conception rate (CR) in inseminated sows, pregnancy rate (PR = recovery rate), treatment-insemination interval (TII) and treatment- pregnancy interval (TPI) within 42 days after the initial examination were evaluated. In addition PR in groups of sows divided according to parity (1-3, 4-6 and ≥ 7) were also evaluated. IR and PR were higher in Group 4 (84.0% and 44.0%) and lower in Group 1 (17.2% and 6.9%) in comparison with the other groups ( P < 0.001 and P < 0.05). CR, TII and TPI did not differ between the experimental groups. PR were similar in sows with different parity. The study proved a positive response in sows with large follicular ovarian cysts to the treatment consisting of 2 administrations of 100 µg GnRH at a 12-hour interval.
The ability of any species to support high hunting pressures depends on its reproductive efficiency. Based on the gross anatomic examination of 208 adult female reproductive tracts, we characterised the reproductive biology of the wild white-lipped peccary in the northeastern Peruvian Amazon. White-lipped peccary apparently bred year round in the northeastern Peruvian
Amazon, and the number of pregnant females was 80 (38.4%). Mean ovulation rate was 2.09±0.47 CLs, and litter size was 1.60±0.49 embryos or foetuses per pregnant female. A phenomenon of embryo migration was observed in the 27.5% of pregnant females. Estimations suggest 0.89 births per year and a yearly reproductive production of 1.42 piglets per pregnant female. Females in the late pregnancy stage showed a higher hunting vulnerability that could be an important restrictive factor for the reproductive efficiency of the wild white-lipped peccary populations in the
Peruvian Amazon.
In the Argentine Chaco, the three species of peccaries (Artiodactyla) are likely affected by habitat destruction and hunting, yet basic information on peccary distribution and status in this region is poorly known. This study identifies human factors associated with relative abundance and distribution of each species. Estimation of relative abundance was based on interviews with local hunters, and variables potentially related to distribution and relative abundance of peccaries were estimated for 153 circular sample sites of 10 km diameter in the Argentine Chaco. Peccaries were found in sites of high forest cover, low human density, far from towns and with low density of roads. After accounting for forest cover and other variables, number of settlements was identified as the main variable negatively associated with relative abundance of the three species, which may be a result of local hunting. Density of roads was also negatively associated with presence of chacoan peccaries. Collared peccary seems to be the least susceptible to human perturbations. It was the most widely distributed and found in a wider range of conditions than the other species. Chacoan peccary was relatively rare. Because colonization and development programs are increasing in the region, areas still uninhabited should be protected, construction of roads controlled, and hunting managed.
As husbandry practices have improved, safe and effective contraception for captive wildlife management has become a necessity. Melengestrol acetate (MGA), a synthetic progestin, is highly effective and has been used in many zoo species. Long-term use of MGA has been associated with uterine lesions in zoo felids, but effects in zoo canids have not been evaluated. This retrospective study documented spontaneously occurring lesions and investigated the impact of MGA on the reproductive health of zoo canids. Reproductive tracts from adult females were submitted by US zoos to the Association of Zoos & Aquariums' Wildlife Contraception Center Health Surveillance Program. Reproductive tracts were sampled and processed for histopathologic examination following standard protocols. Microscopic evaluations were performed without prior knowledge of MGA treatment status. Prevalence of uterine lesions was evaluated and compared between MGA-treated animals (n = 20) and control (untreated) animals (n = 61). Common lesions within the study population as a whole included endometrial hyperplasia (predominantly cystic) (53%), hydrometra (33%), and adenomyosis (25%). Treatment with MGA was a risk factor for endometrial hyperplasia, hydrometra, fibrosis, and adenomyosis. Uterine mineralization occurred exclusively in MGA-treated animals. Results indicate that MGA contraception can lead to lesions that may permanently impair the fertility of females. Therefore, if long-term contraception of zoo canids is necessary, the use of alternate methods of reproductive control such as gonadotropin-releasing hormone (GnRH) analogs or GnRH vaccines that reduce gonadal hormone exposure should be pursued.
This study was conducted in the framework of a program assessing the economic viability of raising collared (Tayassu tajacu) and white-lipped (T. pecari) peccaries in captivity. In collared peccary, previous studies suggested an ovarian or oestrous cycle of 22-24 days. Our results indicated a much longer cycle length. Based on progesterone measurements, ovarian cyclicity averaged 27.8 +/- 1.5 days (range 23-34). The duration of female receptivity, assessed from behavioural observations (acceptation of male mounting), was 4 +/- 2.9 days. Behavioural oestrus was recorded in only 33 of 47 cycles (70.2%). The oestrus detection rate varied individually from 50 to 87%. In white-lipped peccary, average cycle length was 29.7 +/- 0.8 days (range 25-32). Behavioural oestrus was much longer than in the collared peccary (5.7 +/- 4.7 days). The oestrus detection rate averaged 58%. Therefore;in both species, behavioural information, although helpful, is not the most reliable method for detecting the time of ovulation. Measurement of progesterone is a more accurate method. This initial study was based on hormone determination in plasma. Further development will test if non invasive methods -analysis of urinary and faecal steroids -would be easily applicable for the management of breeding herds of peccaries.
Uterine leiomyomata (UL) have a substantial impact on women's health, but relatively few studies have identified opportunities for primary prevention of these neoplasms. Most established risk factors are not modifiable, including premenopausal age, African ancestry, age at menarche, and childbearing history. The main challenge in studying UL is that a large proportion of tumors are asymptomatic. Herein, we review the epidemiology of UL from published studies to date. We highlight the advantages of ultrasound screening studies and the ways in which their innovative methods have helped clarify the etiology of disease. We conclude with a discussion of promising new hypotheses.
During a routine geriatric examination on a 9-yr-old, nulliparous female African warthog ( Phacochoerus africanus ), a severely enlarged, mixed echogenicity uterus was discovered during transabdominal ultrasound. Ovariohysterectomy (OVH) was elected and performed due to concern for a potential neoplastic condition. Postoperatively, the warthog was treated prophylactically with metoclopramide and ranitidine to promote gastrointestinal motility and prevent postoperative ileus. The gross appearance and histopathology confirmed the presence of extensive widely disseminated cystic changes consistent with cystic endometrial hyperplasia (CEH) and multiple para-ovarian cysts. Uterine pathology, including CEH, is a common condition in domestic potbellied pigs ( Sus scrofa ), and as a result, it is recommended to perform an OVH at an early age. The advanced uterine changes may have accounted for this animal's history of infertility. This case provides evidence that nulliparity may be associated with the development of uterine pathology in warthogs. Increased knowledge of reproductive pathology will aid in improved management strategies for breeding nondomestic suids.
We report results of a 2-year field study on the ecology of the endangered Chacoan peccary (Catagonus wagneri) in the Paraguayan Gran Chaco. Stable groups averaged 4.5 individuals. Two intensively tracked groups used ranges of 1,095-1,551 ha by minimum-convex polygons. Animals were active from dawn to dusk, with variations due to season, individual, and temperature. They travelled on average 2.2 km/day, not always returning to the same nightrest position. Ground cacti on which they fed were aggregated in infrequent patches scattered within their habitat of thorn forest. Daily ranges averaged 18.25 ha and were used on ca. 42-day cycles. Core areas were associated with cactus patches. Mutual avoidance between groups was indicated by low overlap of home ranges and the presence of scat stations. A dispersing group of one male and one female occupied three temporally and spatially discrete ranges, and moved 4.6 km over 9 months. The study area contained 0.43 individuals/km2. The population in the study area was in decline, explained by an annual mortality of 47% (five deaths recorded), probably low survival of young, a single farrowing season during the year, and a probable age of 2 years for first reproduction. We discuss implications of these results for conservation of the species.
For over 25 years, the Reproductive Health Surveillance Program has collected, processed, evaluated, and archived reproductive tracts from nondomestic mammals submitted by zoos. The analysis of the data from this archive has been used to recognize lesions associated with exposure to certain contraceptives; but arguably more importantly, to also document naturally occurring lesions. The goals of this program are to enhance the reproductive management of captive and free-ranging species by providing information about the effects of various contraceptives and to provide basic information regarding the natural reproductive histories and naturally occurring lesions in male and female zoo animals.
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 Chacoan peccary (Catagonus wagneri), considered extinct until 1975, lives in the central Paraguayan Chaco in sympatry with the Collared peccary (Tayassu tajacu). A radiotracking study revealed that Chacoan and Collared peccaries kept stable groups with mean sizes of 4.5 and 6.7 individuals respectively. Four Chacoan peccary groups were territorial and had home ranges averaging 1098 ha by convex polygons, and one Collared peccary group had a range of 685 ha. Contact between species entailed agonistic behaviours, but the Collared peccary group shared 75 % of its range with two Chacoan peccary groups. One of these shared 88 % of its range (380 ha) with the Collared peccary group, the parts most frequently used by each species being within the overlapping area. Utilization distributions of each species were more highly correlated than random expectation, in grid-cells of 25 to 7 ha; utilization intermeshed, however, between 3-ha and smaller grid-cells, indicating partitioning at a fine scale of resolution. The probability of meeting was therefore low, but a mean separation of 986 ± 117 m between groups was maintained more frequently than random expectation. Chacoan peccaries were active from dawn to dusk while Collared peccaries rested during the hottest part of the day (c. 40 °C). We discuss the implications of these findings for understanding the ecology of these two species and other members of the large mammalian herbivore guild in the Chaco.
The ability to safely and effectively manage reproduction is central to the success of AZA captive-breeding programs. Although the AZA Wildlife Contraception Center routinely monitors contraceptive safety, there have been no studies that compare the effects of contraceptive use to separation of males from females, the other option for preventing reproduction. We used retrospective medical records and pathology reports submitted by AZA and related facilities for the seven AZA-managed canid species to assess rates of uterine pathology relative to female reproductive life histories. Our results showed that the prevalence of both pyometra and endometrial hyperplasia (EH) was associated not only with treatment with the two most common contraceptives (Suprelorin® and MGA implants) but also with the number of years barren (i.e., not producing a litter and not contracepted). Rates of pyometra and EH were especially high in African painted dogs and red wolves, but lowest in swift and fennec foxes. The number of years producing a litter had a low association, suggesting it could be protective against uterine pathology. A more recently developed Suprelorin® protocol using Ovaban® to prevent the initial stimulation phase, followed by implant removal when reversal is desired, may be a safer contraceptive option. These results concerning the relationship between reproductive management and uterine health have important implications for AZA-managed programs, since the unsustainability of many captive populations may be due at least in part to infertility. Managing a female's reproductive lifespan to optimize or maintain fertility will require a reconsideration of how breeding recommendations are formulated. Zoo Biol. XX:XX-XX, 2013. (c) 2013 Wiley Periodicals Inc.
The Chacoan peccary Catagonus wagneri is endemic to the dry thorn forest of the Gran Chaco of Paraguay, Argentina and Bolivia. Since its discovery by scientists in the 1970s its population has declined due to overhunting, habitat destruction, and possibly disease. As of 1989 about 5000 individuals are estimated to survive in the Paraguayan Chaco. Small dispersed populations still exist in Argentina and Bolivia, but more information is needed on the status of this species in those two countries. In Paraguay, Chacoan peccaries have almost disappeared from the two national parks within their range and the only significant population exists in an area where there are no reserves. The survival of this species depends on enforcing regulations against hunting both within and outside the national parks, translocating animals to the parks, establishing a system of reserves on private land in critical areas, training of Paraguayan wildlife professionals, and environmental education.
Managing reproduction for Canidae species is a challenge for zoological institutions and wildlife sanctuaries. There are four basic options for contraception: separation of sexes, surgical procedures, immunological and hormonal methods. Animal managers face potential challenges for each option, and advantages and disadvantages should be taken into consideration when making a decision. This paper evaluates four common Canidae species with results from hormonal monitoring: Gray wolves Canis lupus/Mexican gray wolves Canis lupus baileyi, Maned wolves Chrysocyon brachyurus, Fennec fox Vulpes zerda and African wild dogs Lycaon pictus. Special focus is given to individuals treated with the gonadotropin-releasing hormone (GnRH) agonist, Suprelorin®. To date there are considerably more data for African wild dogs than other canids, as extensive field observations are available for this species. Therefore, African wild dogs are more extensively covered in this paper. GnRH agonists have been designated the safest reversible method of contraception for carnivores and so continued studies are important. Results outlined below demonstrate individual dosing differences that occur not only across species but also between similar individuals. Although dosing and duration of efficacy still need further investigating, GnRH agonists are still considered to be the safest and most appropriate method available. As evident in this paper, contraception is a much-needed tool for reproductive management.
In the World Zoo and Aquarium Conservation Strategy, the world's leading zoos commit to focusing their efforts on conserving wildlife. Such a commitment is made as human activities are driving many species of wildlife towards extinction. The world's leading zoos aim to act as a counterbalance to activities that undermine the sustainability of wild populations of threatened species. However, to date, this same group of zoos has largely failed to manage its own populations of wildlife sustainably despite distinguished calls to action over the past 25 years, significant scientific input and much organizational effort. This paper explores the efforts of the global zoo community to bring sustainability and conservation value to its animal populations. It looks at where we have come from, where we are now and where we need to go from here.
The aim of this study was to evaluate the relationship between ovarian cysts and concentrations of ovarian steroid hormones: 17beta-estradiol (E(2)), progesterone (P(4)), testosterone (T), and androstendione (A(4)) both in blood plasma and in cysts and morphological state of the ovarian cortex in sows. Females were divided into three groups: PCO (sows with polycystical ovaries), OO (sows with oligocystic ovaries) and control (sows without ovarian cysts). The ovaries for evaluations were collected after slaughtering of 18 multiparous sows. Between the PCO and OO animals, statistically significant differences in numbers of the follicular cysts (FC) (8.6 vs. 1.5), follicular theca-lutein cysts (FTLC) (8.0 vs. 2.0), follicular lutein cysts (FLC) (4.5 vs. 2.0) and corpus luteum cysts (CLC) (1.7 vs. 0.4) (P< or =0.01) were noted. In the PCO sows the most common kinds of cysts were FC and FTLC (8.6 and 8.0) whilst in OO sows the cysts occurred on their ovaries on a similar level (FC - 1.6, FTLC - 2.0, FLC - 2.0). Existence of more than 10 ovarian cysts in the sows significantly decreases the frequency of physiological ovarian follicles (primary, growing and maturing) and significantly increases the pathological process of atresia on all stages of ovarian follicles development (P< or =0.01). The study did not reveal any effect of growing or decreasing number of ovarian cyst on concentrations of E(2) and P(4) in blood plasma of sows. Polycystical ovaries significantly decreased concentrations of A(4) but increased the concentration of T in blood plasma (P< or =0.01). The general presence of ovarian cysts considerably positively correlated with concentrations of E(2), T and A(4) from cysts' fluid, of all kinds of ovarian cysts and atresia of primary follicles (a correlation coefficient r from 0.72 up to 0.97, P< or =0.05). The phenomenon of ovarian cysts significantly negatively correlated with all generations of ovarian follicles (P< or =0.05).
The anatomy and histology of the female reproductive tract of the Indonesian wild pig Babyrousa celebensis was studied by means of reproductive tracts obtained from seven animals aged between two and 22 years of age. The ovary appeared to have the ability to ovulate up to four ova at one time. However, the combined ovarian output seemed to average 1.86 ova. Ovulation can take place at any time from puberty to old age (22 years). The opening to the uterine tube was indicated by a 'flower-like' array of tall, broad epithelial 'petals' arising from the luminal surface of the funnel. The mucosal surfaces of these structures were covered in a mixture of prominent ciliated cells and bulbous secretory cells. The uterine tube followed a tightly convoluted path to the tip of the uterine horn. The uterus was proportionately short. The anatomical construction of the uterus was similar to those of other suids in that the columnar endometrium was heavily folded, there was a rich supply of uterine glands in the lamina propria, and the uterus was provided with a good blood supply. The cervix was thick walled and had a spiral lumen.
Sixteen pregnant collared peccaries were assigned to four experimental diets representing two levels of crude protein and two levels of digestible energy. Serum levels of progesterone, estradiol-17 beta (E2), and glucocorticoids were measured by radioimmunoassay. There was no significant dietary effect (P greater than 0.05) associated with any hormone during gestation. Progesterone did not differ between days 11 and 140 of gestation (X +/- SE = 36.48 +/- 1.11 ng/ml, N = 72), began to decline during the last week prepartum, and continued to decline within 24 hr of birth. Glucocorticoid concentrations remained level throughout gestation (X +/- SE = 6.57 +/- 0.45 microgram/dl, N = 74). E2 levels were low during the first 90 days of gestation, rose significantly (P less than 0.001) from 10.11 +/- 1.73 pg/ml (X +/- SE, N = 8) at Days 81-90 gestation to 49.07 +/- 12.87 pg/ml (N = 3) at 2-4 days prepartum (Days 141-147 of gestation), and declined rapidly to baseline levels within 24 hr of farrowing. Litter size had no effect on progesterone or E2 concentrations. There was no significant dietary effect on litter size or gestation length. During lactation, glucocorticoids and E2 remained stable and did not differ by diet, while progesterone concentrations appeared to be affected by diet. Individuals on the high energy-high protein diet returned to normal ovarian function before animals on the other three diets. Results indicated that the pregnant collared peccary can maintain a reproductive steroid environment that allows for fetal development in the face of moderate caloric or protein restriction and that the lactating peccary can undergo a postpartum ovulation in the presence of good nutrition.
Melengestrol acetate (MGA) contraceptives are widely used in zoo felids to regulate fertility and may have deleterious effects on endometrial health. To determine whether MGA exposure was associated with endometrial disease, the genital tracts of 212 zoo felids (99 MGA treated and 113 control) representing 23 species were evaluated. Adenomatous and cystic hyperplasia were prevalent in both MGA-treated (85%) and control (61%) groups, and the risk of developing these lesions increased with age. Treatment with MGA further increased the risk of developing advanced hyperplasia regardless of dose, and treatment for >72 months significantly elevated that risk, whereas parous animals had a lower risk. Endometrial polyps, fibrosis, adenomyosis, and hydrometra occurred in both MGA-treated and control animals. MGA treatment was associated with an increased risk of hydrometra and mineralization but not of adenomyosis, polyps, or fibrosis after adjusting for advanced hyperplasia. Acute or chronic endometritis were associated with advanced hyperplasia but not with MGA treatment. These results indicate that proliferative and inflammatory endometrial lesions are common spontaneous diseases in zoo cats, and MGA contraceptives increase the risk of some diseases. The association of MGA with endometrial lesions that could impair fertility should be considered when using this contraceptive in genetically valuable felids.
A 9-yr and 3-mo-old captive female coati (Nasua nasua) was implanted with melengestrol acetate for contraception for 4.5 yr prior to presentation. During her annual examination, purulent vaginal discharge and a palpably prominent uterus were identified. Ancillary diagnostic tests including hematology, cystocentesis, radiographs, and abdominal ultrasound were consistent with pyometra. An ovariohysterectomy was performed and histologic examination revealed pyometra and uterine adenocarcinoma, similar to pathology that has been associated with melengestrol acetate contraception in felids, canids, and primates. Given the potential association between melengestrol acetate and uterine pathology in this case, we recommend caution with melengestrol acetate use in procyonids.
The aim of this work was to determine the incidence of ovarian cysts in the breeding herd and their consequences in the reproductive performance of the herd. Data from 1990 cyclic sows from two farms, with 0-12 parities, lactation length between 6 and 47 days and weaning-estrus interval between 0 and 32 days were evaluated by ultrasound examination for cyst incidence. As cyst was considered an anaechoic structure with smooth and thin walls with a diameter larger than 2 cm that remained visible for at least 5 days after estrus onset. Cyst incidence was found to be 2.4%. Sows with ovarian cysts have a greater return to estrus rate (34.0 x 7.7%, P<0.01), and cysts were associated with around 10% of regular and irregular return to estrus patterns on both farms. The adjusted farrowing rate (52.2 x 90.0%, P<0.01) and anestrual sows that were not pregnant (10.6 x 0.6%, P<0.01) were also influenced by the appearance of ovarian cysts, but they did not influence litter size (P>0.05). The incidence of cysts was not influenced by parity (P>0.05). Sows with shorter lactation had a greater incidence of cysts (P<0.05). Sows with a weaning-estrus interval shorter than 3 days had a greater incidence of ovarian cysts (P<0.05). The time of the year had no influence on the incidence of ovarian cysts (P<0.05).
Problems attributable to long-term captivity have been identified and are responsible for the difficulties in establishing successful reproduction in captive populations of wildlife, specifically, elephants and rhinoceroses. Historically, non-reproductive periods of 10-15 years in nulliparous female rhinoceroses and elephants have not been considered problematic. New evidence suggests that prolonged exposure to endogenous sex steroids and that long stretches of non-reproductive periods induce asymmetric reproductive aging in captive animals. The consequences are reduced fertility, shortened reproductive life-span and, eventually, irreversible acyclicity. Although age-related reproductive lesions have also been documented in male rhinoceroses, they continue to maintain a longer reproductive life-span than females. Since human and domestic animal models have already indicated that early pregnancy provides natural protective mechanism against asymmetric reproductive aging processes and premature senescence, it is imperative that appropriate counter measures such as assisted reproductive technologies (ART) be utilized to ensure early pregnancy in captive animals for their preservation and to ensure increased genetic diversity of the captive populations.
Endometrial cancer is the most common gynecologic malignancy in the United States. The mean age at diagnosis is 61 years; however, 5-30% of women are aged younger than 50 years at the time of diagnosis. The objective of this study was to conduct a clinical and pathologic review of endometrial cancers diagnosed in premenopausal women aged younger than 50 years, to better identify the risk factors for this subgroup of women.
We conducted a retrospective cohort study of patients with histologically confirmed endometrial cancer treated at the University of Texas, M. D. Anderson Cancer Center from 1989 to 2003. Clinical characteristics including age, body mass index (BMI), parity, diabetes, and personal or family history of cancer were obtained from the medical record. Pathologic information was obtained from pathology reports.
Twelve percent (188/1531) of all patients with endometrial adenocarcinoma were aged younger than 50 years. The mean age at diagnosis was 41 years (range 21-49 years). Mean BMI was 34 kg/m(2) (range 18-68); 58% of patients had a BMI of 30 or greater. Fifty-five percent were nulliparous and 39% reported irregular menstrual cycles. The incidence of both diabetes and hypertension was 23%. Thirty-six patients (19%) had synchronous ovarian cancers.
We found that the majority of patients diagnosed with endometrial cancer at a young age were obese and nulliparous. In addition, we found a high incidence of synchronous primary ovarian cancers in this cohort of young, premenopausal women.
The objectives of this study were to analyse faecal steroid metabolites in African and South East Asian pig species kept in European zoos. Species studied were the warthog (Phacochoerus africanus), the red river hog (Potamochoerus porcus) and the babirusa (Babyrousa babyrussa). Faecal samples were collected 1-3 times per week from non-pregnant and pregnant captive female warthogs (n = 9), red river hogs (n = 7) and babirusas (n = 5). Enzyme-immunoassays for faecal progesterone, androgen, and oestrogen metabolites, were tested for their ability to determine follicular and luteal phases. In all three species, oestrous cycles could be monitored with 20alpha-OH- and 20-oxo-pregnane assays. In contrast, oestrogens and androgens were not useful in characterising follicular activity during the oestrous cycle in any species. Faecal 20alpha-OH- and 20-oxo-pregnane values were significantly correlated. Faecal pregnane concentrations revealed species-specific differences. Luteal phase values of 20alpha-OH-pregnanes were considerably higher than 20-oxo-pregnanes; 20alpha-OH-pregnanes were in the range of 3-10 microg/g in warthogs and red river hogs, whereas concentrations were 30-200 microg/g faeces in the babirusa. Regular oestrus cycles had a length of about 35 days in all three species studied. Results indicated a seasonal influence on the occurrence of reproductive cycles in the warthog with anoestrous periods in the European summer. The red river hog was found to be a seasonal and poly oestrous breeder; oestrus cycles started by January and continued until summer. In contrast, the babirusa showed non-seasonal ovarian cyclicity. In pregnant red river hogs, progesterone metabolites were comparable to luteal phase values of the oestrous cycle during the first 3 months of gestation, but did further increase during the last month of pregnancy. Oestrogens and 17-oxo-androstanes were significantly elevated during the second half of gestation. In summary, the reproductive biology of three exotic pig species was studied using non-invasive faecal steroid analysis and these methods were used for comparative investigations of oestrous cycles, pregnancy and seasonality.
Contraceptives are used for reversible reproductive control in genetically valuable wild felids, as permanent reproductive control in generic wild felids, and as an economically practicable means to control feral cats. The progestin contraceptives, megestrol acetate, melengesterol acetate, medroxyprogesterone acetate, and levonorgestrol (administered orally, in implants, or as depot injections), are effective in preventing pregnancy. However, long-term use is associated with endometrial hyperplasia, endometrial cancer, and mammary cancer. Gonadotropin releasing hormone analogs or luteinizing hormone vaccines that achieve contraception by suppressing ovarian or testicular function, do not have the adverse health effects of progestins. However, reliable reversibility has not been demonstrated, and male secondary sex characteristics may be suppressed. Bisdiamines also inhibit spermatogenesis and lower circulating testosterone concentrations in treated male cats. Porcine zona pellucida vaccines are ineffective contraceptives in felids and may cause serious health problems when combined with some adjuvants. Because of the limited availability of non-progestin contraceptives and side effects associated with some agents, widespread application of contraception to felids has been curtailed. More non-steroidal methods of contraception should be tested in the future to provide alternatives for controlling reproduction in felids. Furthermore, all empirical information on contraceptive safety and efficacy should be assembled in a database to provide the knowledge needed by veterinarians and managers to determine benefits/risks of currently available contraceptives in felids, both domestic and wild.
Most captive female elephants are nulliparous and aged and many have endometrial disease, factors that may hinder fertility. This study characterized the pathologic features and demographic distribution of endometrial lesions from 27 captive Asian (Elephas maximus) and 13 African elephants (Loxodonta africanus), 12- to 57-years of age. The principal lesion was marked cystic and polypoid endometrial hyperplasia (CEH), present in 67% of Asian and 15% of African elephants ranging from 26 to 57 years. The lower prevalence in African elephants likely reflects their younger age range in this study. Fourteen of 15 affected elephants with breeding information were nulliparous. These results suggest that CEH and polyps are common in aged nulliparous elephants, and the severity of these lesions may impair fertility. These findings will be useful in the interpretation of ultrasonographic findings during reproductive examinations of potential breeding cows. Also, breeding programs should focus on younger animals.
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The Chacoan peccary (Catagonus wagneri)
- Taber
Reproductive behaviour and development of the young of the chacoan peccary (Catagonus wagneri Rusconi, 1930) in the Paraguayan Chaco
- Brooks
Captive management of tagua (Chacoan peccary) in Paraguay
- Kingswood
The anatomy and histology of the reproductive tract of the male Babirusa (Babyrousa celebensis)
- Ziehmer
Euthanasia: a nettle we need to grasp
- Richardson