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    Spatially restricted occurrence and low abundance as key tools for conservation of critically endangered large antelope in West African savannah

    Based on the extensive camera trap study, the very first information about the occupancy, trapping rate, activity pattern, group size, social structure and vital rates of the critically endangered Western Derby eland in its last refugium, the NKNP in Senegal, is presented here. The first estimation of abundance since 2006 is also provided7.Spatiotemporal behaviour pattern of WDE in the parkThe results of the CT survey in the NKNP highlight the substantially lower occupancy and trapping rate of WDE in comparison to other large ungulates in the park. According to the current results, the WDE occupied less than 5% of the park area during the dry season, being exclusively within the zone of Mont Assirik, and more specifically the Mansa Fara marsh, which can be thus designated as the core area of the WDE distribution. The trapping rate of the roan antelope, which is considered the most abundant antelope species in the NKNP, was 4.04, i.e. more than 11 times higher than that of WDE in the present study. Even the Western hartebeest, which is considered a rare species in the NKNP, had a trapping rate of 0.61, which is ca. twice as high that that of the WDE (see Rabeil et al.8 for further details, and additional ungulate species).In the zone of Mont Assirik, the trapping rate of WDE increased to 2.42, but the trapping rates of other antelope species remained higher still (4.6 for roan antelope and 3.39 for Western hartebeest8). The WDE distribution is therefore strongly localised within an area which seems to also be attractive for the other species, including the incidental records of elephant. The Mont Assirik zone, and more specifically the Mansa Fara marsh area, is therefore the crucial zone within the park for the WDE, and it appears to support a larger number of other antelope species as well. This zone should therefore be considered as a key conservation area, potentially very sensitive to targeted poaching, and thus crucial for efficacy of targeted law enforcement actions.When looking at the diurnal activity pattern, the WDE were active before midnight, approximately 3 h after sunset, in the morning, approximately 2 h after sunrise, and then again in the afternoon, with the peak activity during the hottest part of the day. This activity pattern is different from the typical bimodal activity pattern, which has peaks at dawn and dusk, as reported for most African grazing and browsing herbivores, seen as a behavioural thermoregulation strategy to avoid heat stress41,42,43. Instead, the WDE, being a large body-sized browsing antelope19,44, must stay active throughout the day to seek discretely distributed food, and fulfil foraging requirements by feeding while moving. The WDE appears to be well-adapted to tolerate such high temperatures, similar to kudu45, roan46, and giraffe47. Such behaviour pattern enable the law enforcement patrols, as well to tourists, to detect herds of WDEs and monitor them, thereby increasing their protection against poaching.Individual identification and recapturesThe individual identification of animals was more successful during the daytime, as the light conditions mostly did not allow for the proper visualization of the stripes on the flanks during the night captures (as similarly reported in Jůnek et al.18). When the ID is targeted to be successful during the night (as for the leopards and tigers), the camera traps are often set to the video mode to ensure a higher possibility of identification48. However, the activity of the WDE is not predominantly nocturnal, and the captures were distributed over both the daylight and night hours, and therefore the results are considered representative for the whole period.The AD animals were more likely to be identified in the present study because of their larger body size, resulting in better visibility of their stripes. The higher identification rate of larger individuals also likely contributed to the higher probability of recaptures, which were only recorded for individuals of 2Y and older.Overall, the identification success rate was comparable, maybe even slightly higher, than the previous camera trap study performed on the Eastern Giant eland in Chinko, CAR, specifically in the dataset from the dry season13, which corresponds to the observation period in the present study as well.In the NKNP, recaptures of individuals were recorded, whereas there were none reported in Chinko13. The recapture rate of the WDE in NKNP, with mostly short distances between the capture-recapture sites, even after the long-time gaps between the captures, confirm again that the WDE likely inhabit a relatively limited area of the park.Group size and social structureThe mean group size recorded in the NKNP during the present study was slightly larger than that within Chinko; however, the maximum group size was smaller in NKNP (32 vs. 41 individuals). Mixed herds were the largest in terms of the number of individuals, in both studies. The average group size has been reported as 20–30 individuals49, but Derby elands may form large herds of over 100 individuals in the late dry season14. Similarly, a large herd was reported within NKNP in 2006, having 69 individuals7, and a herd of around 60 WDE was also recently reported by patrols in 2020 (GIE Niokolo, personal communications). It is important to highlight that the results from the present study reflect the number of individuals per event based on visible individuals within the scope of the camera, and that the real group sizes may actually be larger.No adult males were present in the mixed herd in two cases within the present study; however, there were always 2YM and a few unidentified individuals, suggesting that the herd should not be considered as a pure “nursery herd”, as known for sexually dimorphic antelope species50.Calves are born in the NKNP during the period comparable to that of Bandia, Fathala and Chinko, i.e. during the early dry season16. The higher proportion of calves in the dry season corresponds with the nursing period of six months for WDE44. Given a pregnancy length of nine months, the WDE mating season in NKNP peaks in January/February, which also corresponds with the formation of large herds with multiple males, as similarly seen in Chinko and Cameroon13,14.Vital ratesThe sex ratio of the WDE in the NKNP was female-biased. The skewed adult sex ratio reflects the lower survival rate of males in comparison with females, typical for polygynous species51. This result also corresponds with the findings from other Derby eland populations, namely from Chinko, where the bias towards females in the adult sex ratio was even more pronounced (0.67:113). A similar ratio was found in the hunting reserves within Cameroon35, but also in the semi-captive population, without hunting and without predators34. As the ratio in NKNP was less skewed than that within Chinko and Cameroon, a lower or zero selectivity for males by hunters/poachers is expected.The population of WDE in the NKNP showed a lower proportion of adults versus other age categories compared to the demographic structure of the WDE in the semi-captive breeding facilities of the Bandia and Fathala reserve33,52, and to those of the Eastern subspecies of Derby eland in the Central African Republic13 (see Table 3). The data from the present study also showed a surprisingly high breeding rate (likely close to 100%), as well as a high survival rate of yearlings. This combination of demographic characteristics should be highly favourable, and likely to lead to a significant population growth rate; however, this does not seem to be the case of the WDE population in the NKNP (please refer to further discussion about population size).In this context, the population of WDE in the NKNP was explored deeper, to examine possible scenarios of changes within the population structure. The changes in vital rates between two years of monitoring (2017 and 2018) were examined, by taking advantage of the possible recognition of the age category until two years of age, and the knowledge of the life tables of the enclosed, non-predated WDE population in the Bandia reserve34. Life tables were created for each year, and for males (M) and females (F) separately, according to the standard structure2, and based on two scenarios: a) only the observed number of JUV and 1Y (nx), and modelled 2Y (model ‘JUV + 1Y’); b) the observed number of JUV and 2Y (nx) (model ‘JUV + 2Y’). Then, estimations of animals in age categories based on two parameters were calculated: (i) based on the mortality rate (qx) known from the Bandia reserve (Senegal), and (ii) based on the recorded number of animals (NAD), to calculate the estimation of mortality rate (for details, see Additional file 1: Table S2).The resulting values demonstrated that with survival rates comparable to a population without predation and poaching, the number of adults would be twice or three times higher than currently detected in the present study. Yet, considering the recorded number of adult individuals, the annual adult survival rate was considerably low, i.e. 59–69% in males and 67–82% for females. To conclude, the demographic structure of WDE in NKNP showed a high breeding rate, moderate juvenile survival, high survival rate of yearlings, and a low survival rate of adults.Juvenile survival is one of the most fluctuating vital rate parameters, sensitive to population density, stochastic environmental variation, and predation53,54,55. Given the high proportion of juveniles within the population, and the breeding rate higher than that in Cameroon (74%14) and within the captive population (77%34), the juvenile survival rate does not seem to negatively affect the population growth in the NKNP. High breeding rates could be a more robust determinant of population change than AD mortality53, and it is therefore possible that the WDE population size is stable in the NKNP, or even increasing, despite the low adult survival rates. On the other hand, the relatively low numbers of AD individuals in the population indicates low survival rates, which may lead to the decline and final crash of the population54. It is acknowledged that data from two consecutive years was used in the present study, which were not comparable due to different CT settings, and that long-term monitoring, which accounts for variability in vital rates, would be a conservation essential to identify the trend and population change.Based on the present findings of WDE spatiotemporal behaviour and estimates of vital rates, several explanations about multiple processes interacting in the environmental, anthropogenic and conservation context of the park, which inherently affect the small population of WDE, can be inferred. One explanation may suggest that a low proportion of AD WDE and higher JUV survival rates may reflect the influence of growing populations of apex predators in the NKNP, specifically the population of lions56, which may preferentially target the adult individuals57. The age-sex structure also encourages the interpretation that the adult animals are exposed to human-related factors, which prevents them from expanding from the core area of their distribution, exacerbating male-male competition in the limited space34. The poaching activity was also highlighted as an existing threat to WDE populations35. However, law enforcement has been substantially intensified in the core and south-eastern part of the NKNP since 201758, and lion-conservation actions are specifically supported. Thus, the predator populations may have started to grow, which is confirmed by the relative high trapping rate of lions in this core area8. Hence, increased predation may interfere with other environmental factors and consequently affect the WDE population dynamics at the level of AD individuals55,59.A complementary scenario may highlight other factors, specifically, those which maintain the WDE population within a certain spatial extent of the park, i.e. Mont Assirik and Mansa Fara marsh zone. This area can be delimited either ecologically by specific unidentified resources, or by anthropogenic factors, namely a highly frequented trade road crossing the park, wild bushfires, and intensive livestock encroachment in a large band from the borders of the park, inwards (up to 10 km). There is also a vast area in the central part of the park that offers an important space with a supposed carrying capacity for large herbivore populations. This area is, however, outside of the zone of intensified law enforcement, and suffers from inadequate surveillance in the long-term, due to the absence of tracks and therefore being difficult for rangers to access. This area certainly represents an attractive zone for targeted illegal hunting actions. These limiting factors constrain large mammals to concentrate within the zone of Mount Assirik and Mansa Fara marsh, which, in turn, makes animal populations vulnerable to any potential environmental or man-induced incidents, like bush fire.Population sizeThe estimated population size of 195 individuals corresponds with the range of most recent estimates of the WDE population size in the NKNP, i.e. 100–200 (approximately 170) individuals6,7,60. Given the fact that the model contains only the data for AD animals (as no other age category had recapture records), it may be considered that this estimate refers to the number of adult individuals in the population. With regards to Table 3, showing that adults are likely to form 43 to 44% of the whole population, it may be inferred that the actual number of WDE in the NKNP could be higher, even up to 300 individuals, if the data are corrected for the 22% of unidentified individuals. The WDE density estimate of 0.138 individuals/km2 was comparable to densities of Eastern Derby eland in CAR (densities ranging between 0.04 and 0.16 individuals/km2), in Chinko13, and ranging between 0.002 and 0.1 individuals/km2 in the northern CAR61, as well as in Cameroon, with densities ranging between 0.002 and 0.08 individuals/km262. On the other hand, in comparison to other antelope species, the estimated WDE density falls within the range of densities of large herbivores reported from many other sites in African protected areas63, where lower values correspond to the larger areas and are also associated with large browsers, i.e. to the type of diet. Maximum densities of a healthy undisturbed DE population were estimated at about 0.5 individuals/km249, and can reach up to 1.19 individuals/km2 in intensively surveyed hunting zones in Northern CAR61. Thus, the density of WDE in the NKNP could be potentially higher. More

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    Conserved ancestral tropical niche but different continental histories explain the latitudinal diversity gradient in brush-footed butterflies

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    Why stem cells might save the northern white rhino

    OUTLOOK
    29 September 2021

    Why stem cells might save the northern white rhino

    Biologist Jeanne Loring explains how her work could bring endangered animal species back from the brink.

    Julianna Photopoulos

    Julianna Photopoulos

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    Stem-cell researcher Jeanne Loring in her laboratory at Scripps Research.Credit: Nelvin C. Cepeda/SDU-T/Zuma/eyevine

    Up to one million plant and animal species face extinction, many within decades, because of human activities. One of these is the northern white rhinoceros (Ceratotherium simum cottoni). Only two individuals remain, both of them female, making the subspecies functionally extinct. Jeanne Loring, a stem-cell biologist and founding director of the Center for Regenerative Medicine at Scripps Research in La Jolla, California, spoke to Nature about how collecting and reprogramming stem cells could save this species and others from extinction.What does stem-cell research have to do with saving endangered animals?Induced pluripotent stem (iPS) cells, which closely resemble embryonic stem cells, can develop into any tissue in the body, including sperm and eggs. The hope is to generate these reproductive cells from the reprogrammed stem cells of endangered animals, and use them in assisted captive-breeding programmes to rescue the species.How did you get involved in this work?My laboratory set out to make iPS cells from endangered animals in 2008, after we visited the San Diego Zoo Safari Park in California. The previous year, a team led by Shinya Yamanaka, who won a Nobel prize for the work, had become the first to make human iPS cells from skin cells called fibroblasts1, and we had immediately started making them too, to treat neurological diseases. The San Diego Zoo’s Institute for Conservation Research had been collecting and freezing fibroblasts from animals since the 1970s. The institute’s director of conservation genetics, Oliver Ryder, was thinking of using stem cells to try to treat musculoskeletal disorders, but nobody had created iPS cells from endangered species before.
    Part of Nature Outlook: Stem cells
    In 2011, my postdoctoral fellow Inbar Friedrich Ben-Nun was the first to reprogramme stem cells in two animals from endangered species: the northern white rhino and the drill monkey (Mandrillus leucophaeus)2. We’re now focused on saving the northern white rhino — Ryder’s favourite animal — but the techniques we are working on are going to become a standard way of rescuing species from extinction.When did this become a serious venture?Our endangered-species project mostly remained a hobby until 2015, when scientists and conservationists from around the world met in Vienna to explore how cell technologies might aid conservation. We seriously discussed the idea of using stem cells to rescue endangered species, and later published a rescue plan for the northern white rhino3. To begin with, embryos will be created from sperm and egg cells that were collected and stored. They’ll then be implanted into a surrogate mother, a southern white rhino (Ceratotherium simum simum). But we want to be able to create more sperm and eggs from iPS cells and implant them, too — and that’s where our team comes in.After the Vienna meeting, the San Diego Zoo invested in this idea. Staff there built a stem-cell lab and the Rhino Rescue Center, where they brought in six southern white rhinos from Africa, specifically to serve as surrogate mothers for embryos made from northern white rhinos’ cells. The animals should be compatible because southern white and northern white rhinos are closely related, and so have similar reproductive physiologies. A team of reproductive biologists led by Barbara Durrant is now working to perfect the techniques to fertilize eggs in vitro and transfer viable embryos into the southern white rhinos.What progress have you made in creating northern white rhinoceros iPS cells?When we first set out to make the cells from endangered animals, we assumed that human versions of the reprogramming genes would not work in a rhino. So we tried reprogramming the rhino’s fibroblasts with horse genes — the horse is one of the closest relatives of the rhino — but this failed. Surprisingly, the corresponding human genes did work, and we were able to generate pluripotent cells. However, we had used viral vectors to reprogramme the cells, and this has been shown to lead to tumours in mice, so it could not be used for reproduction purposes.After three years of tweaking the technique, we were able to perform the reprogramming without any genetic modification. It’s all trial and error — you just have to keep testing different combinations of variables. Earlier this year, we celebrated a milestone in our efforts to rescue the rhino: Marisa Korody’s lab at the San Diego Zoo was able to reprogramme frozen cells from nine northern white rhinos and two southern white females to become iPS cells4.

    Najin (right) and her daughter Fatu are the world’s only remaining northern white rhinos.Credit: Tony Karumba/AFP via Getty

    How do you hope to create gametes from iPS cells?The major effort now is to make eggs that can be fertilized with sperm collected from adult males. We’re following in the footsteps of other researchers who have had success, mainly with mice so far. For example, in 2016, Katsuhiko Hayashi and his team at Kyushu University in Fukuoka, Japan, artificially engineered egg cells from reprogrammed mouse skin cells, entirely in a dish, and these were used to birth pups that were healthy and fertile5.That technique required ovarian tissue to be co-cultured with the developing eggs to get them to mature, and it’s impossible to get that kind of tissue from rhinos without putting them at risk. But in July, the same team showed that it could make both egg cells and ovarian tissue from iPS cells, which was a huge improvement6.We are now trying to find an efficient way to make the precursors of gametes, known as primordial germ cells, from the iPS cells of northern white rhinos. We know it’s possible — we’ve seen it happen spontaneously in cultures of these iPS cells — but we need to learn how to generate more of them. And then we have to turn those germ cells into eggs and sperm — or at least, something like sperm. Typically, the process of in vitro fertilization (IVF) involves knocking the tail off a sperm cell and injecting the small head directly into the egg, so we might not need to make sperm with tails. The IVF process itself will need to be adapted, however, to the southern white rhino surrogates — we don’t know for sure that it will work as it does in humans, because it’s never been done before.What advantage is there to using stem-cell technology over other approaches, such as cloning?The San Diego Zoo has frozen fibroblasts from 12 northern white rhinos. We didn’t want to clone those animals, because we would still have only the same 12 individuals. But if we make gametes from them instead — sperm from males, eggs from females and, in theory, sperm from females — then we could make various combinations through IVF to get a new, genetically diverse pool of animals that will help the species to survive. We have found that there is sufficient diversity in combining that group of 12 to exceed the diversity of the current population of southern white rhinos.
    More from Nature Outlooks
    Another group, at the Leibniz Institute for Zoo and Wildlife Research in Berlin, is instead harvesting eggs from the two living animals in the hope that they can fertilize them and get new animals that way. I’m perfectly happy if that works, but the challenge is getting enough diversity in the population if you have eggs from only one or two animals.Have you encountered opposition to your iPS-cell-mediated approach?If I were doing this with humans there’d be a lot of debate, but with animals there is less. One criticism is that resources for conservation should be invested differently, for example in restoring natural habitats and educating people. One argument we hear is that there’s no purpose in rescuing a species that will be confined to zoos because of poaching. I don’t know how to stop people from hunting rhinos for their horns, but I will do what I can to try to save an animal that humans have forced into extinction.Are you confident that your work will help to save the northern white rhino?It saddens me that as we’ve made progress in the lab, these animals have been dying out. When we started this project there were 8 of them alive, and now there are only 2: Najin, aged 32, and her daughter Fatu, aged 21, who live in a protected park in Kenya. It’s possible that these last two survivors will be gone by the time we succeed. I hope that’s not the case, but we’re working with cells that have been harvested and frozen, so we can try to bring the species back to life if necessary.I can’t predict how long it will take to get there — things have happened much more slowly than I’d like. But I do hope that our efforts will pay off over the next 10 to 20 years. I want to see a new northern white rhino in my lifetime — before I become ‘extinct’!

    Nature 597, S18-S19 (2021)
    doi: https://doi.org/10.1038/d41586-021-02626-zThis interview has been edited for length and clarity.This article is part of Nature Outlook: Stem cells, an editorially independent supplement produced with the financial support of third parties. About this content.

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