Modelling the effectiveness of contraception for controlling introduced populations of elephant in South Africa

Re‐introduced African elephant (Loxodonta africana Blumenbach) populations are growing at very high rates in many of southern Africa’s reserves, have attained densities higher than previously thought possible and may be exhibiting irruptive growth. Active management of such populations is necessary to prevent the potentially negative effects on habitat and biodiversity that are associated with elephant overpopulation. One potentially feasible method of elephant management is immunocontraception, but very little is known about the long‐term effectiveness of this method. Using demographic data from three South African elephant populations, we made model projections of the effects of contraception on population growth rates to determine whether contraception may be a feasible management tool for elephant. In comparison with noncontracepted populations, realistic reductions in population growth rate after 20 years of contraception were projected to be up to c. 64%, with 50% being a very feasible target. Through its ability to reduce population growth rates, immunocontraception should be an effective tool for preventing or minimizing irruption in elephants and, perhaps, other introduced ungulate species.     

Preliminary evaluation of porcine zona pellucida (PZP) immunocontraception for behavioral effects in feral horses (Equus caballus)

Successful management of captive populations of wild animals requires effective control of reproduction. Contraception is one tool for controlling reproduction of animals in zoos; however, the options available to the animal manager are limited. Contraceptives vary in efficacy, reversibility, and side effects, and thus may not be suitable for widespread use. One consideration when selecting a contraceptive is its potential for side effects on behavior, especially given the fact that reproduction plays such a prominent role in the biology of any species. To date, there have been few evaluations of contraceptives for behavioral effects, and those that have been conducted have focused on hormone-based contraceptives. This study sought to evaluate a novel method of population control, immunocontraception, for behavioral effects in a population of feral horses. Porcine zona pellucida (PZP) immunocontraception prevents fertilization of ova and does not alter normal hormone secretion patterns. It therefore should leave the animal behaviorally intact in terms of reproductive behavior. The study examined the behavior of 43 sexually mature mares on Assateague Island during the 1997 breeding season and, with help from Earthwatch volunteers, collected observations over a 3-month period. The study found no significant differences between treated and untreated mares in general activity budget, aggression given or received, and spatial relationships relative to the stallion. These preliminary findings indicate that PZP contraception seems to have no acute behavioral effects on the behavior of individuals. The study findings also suggest that PZP could be a desirable and effective management tool for captive species in which social behavior plays an integral role in group dynamics. Analyses of group level effects and population level effects are continuing.     

Predicting the efficacy of virally-vectored immunocontraception for managing rabbits

Models were developed to examine the efficacy of immunocontraception as an alternative control method for pest rabbits. The models simulated the dynamics of rabbit populations structured by age and sex, and helped identify the benefits of an integrated pest management strategy that includes immunocontraception and lethal control. Virally vectored immunocontraception (VVIC) using a sterilising myxoma virus reduced the long-term density of rabbits. However, our models indicated that the efficacy of VVIC is much less than using lethal methods of management currently available (e.g. poison baiting). Nevertheless, in areas where lethal control cannot be used, a sterilising strain of myxoma may be a useful tool for rabbit management, but competition between sterilising and non-sterilising strains will reduce the overall efficacy of VVIC. Regardless of how effective poisoning is at reducing rabbit numbers, the benefits in terms of increased pasture availability and wool growth may not outweigh the costs incurred by a poisoning campaign. In our analysis the most cost-effective control remains natural epizootics of myxomatosis since they do not incur a cost to the landholder. There is likely to be some small additional benefit to releasing a sterilising strain of myxoma, and landholders may need to supplement this with baiting under some circumstances (e.g. above average breeding season or areas where myxomatosis occur infrequently).     

Demographic Variables for Wild Asian Elephants Using Longitudinal Observations

Detailed demographic data on wild Asian elephants have been difficult to collect due to habitat characteristics of much of the species’ remaining range. Such data, however, are critical for understanding and modeling population processes in this endangered species. We present data from six years of an ongoing study of Asian elephants (Elephas maximus) in Uda Walawe National Park, Sri Lanka. This relatively undisturbed population numbering over one thousand elephants is individually monitored, providing cohort-based information on mortality and reproduction. Reproduction was seasonal, such that most births occurred during the long inter-monsoon dry season and peaked in May. During the study, the average age at first reproduction was 13.4 years and the 50^th percentile inter-birth interval was approximately 6 years. Birth sex ratios did not deviate significantly from parity. Fecundity was relatively stable throughout the observed reproductive life of an individual (ages 11–60), averaging between 0.13–0.17 female offspring per individual per year. Mortalities and injuries based on carcasses and disappearances showed that males were significantly more likely than females to be killed or injured through anthropogenic activity. Overall, however, most observed injuries did not appear to be fatal. This population exhibits higher fecundity and density relative to published estimates on other Asian elephant populations, possibly enhanced by present range constriction. Understanding the factors responsible for these demographic dynamics can shed insight on the future needs of this elephant population, with probable parallels to other populations in similar settings.     

Population dynamics of the African elephant (Loxodonta africana)

Recent studies on elephant populations from East Africa and from Zambia have suggested that as population density increases, so does the mean age at puberty and the mean calving interval. At the same time there is also an increase in the proportion of old females that are reproductively inactive. By constructing elephant population models, it is possible to investigate the extent to which these "homeostatic mechanisms" will regulate an elephant population. The models indicate that a change in the duration of the calving interval is more important as a population regulating mechanism than a change in the age at puberty, and that the proportion of old reproductively inactive females is of little significance. The importance of neonatal mortality in controlling population growth is emphasised by the models, and they also show that an annual population increase of 4% would be close to the maximum value.     

Demography of a population with a long history of poaching and the utility of the individual identification technique as a tool for monitoring intermittently studied elephant populations

In many elephant populations in Africa, adverse effects of poaching including altered age and sex structure and long calving intervals continue to negatively impact the rate of recovery. The study reported here characterized the demographic status of the elephant population in Meru National Park, Kenya, so as to determine the size, age and sex structure, and calving interval of the population and to compare its demographic parameters against those from the relatively stable elephant population at Amboseli. Additionally, a demographic study conducted 7 years earlier enabled us to determine the demographic performance of the population and to explicitly test the utility of the individual identification technique in monitoring intermittently studied populations. We found 392 elephants in the park. The proportion of older individuals was lower, and the calving interval was longer than estimates from Amboseli. We recognized 16% of elephants indexed in the previous study. Our results suggest that the individual identification technique may be useful in monitoring demographic changes including poaching in intermittently studied elephant populations. Overall, our results suggest that although the Meru elephant population showed signs of recovery, poaching continues to imperil its recovery.     

Pedigrees and the Study of the Wild Horse Population of Assateague Island National Seashore

ABSTRACT Recently, a number of papers have addressed the use of pedigrees in the study of wild populations, highlighting the value of pedigrees in conservation management. We used pedigrees to study the horses (Equus caballus) of Assateague Island National Seashore, Maryland, USA, one of a small number of free-ranging animal populations that have been the subject of long-term studies. This population grew from 28 in 1968 to 175 in 2001, causing negative impacts on the island ecosystem. To minimize these effects, an immunocontraception program was instituted, and horse numbers are slowly decreasing. However, there is concern that this program may negatively affect the genetic health of the herd. We found that although mitochondrial DNA diversity is low, nuclear diversity is comparable to that of established breeds. Using genetic data, we verified and amended maternal pedigrees that had been primarily based on behavioral data and inferred paternity using genetic data along with National Park Service records of the historic ranges of males. The resulting pedigrees enabled us to examine demography, founder contributions, rates of inbreeding and loss of diversity over recent generations, as well as the level of kinship among horses. We then evaluated the strategy of removing individuals (using nonlethal means) with the highest mean kinship values. Although the removal strategy increased the retained diversity of founders and decreased average kinship between individuals, it disproportionately impacted sizes of the youngest age classes. Our results suggest that a combined strategy of controlled breeding and immunocontraception would be more effective than removing individuals with high mean kinships in preserving the long-term health and viability of the herd.     

Individual heterogeneity in life-history trade-offs with age at first reproduction in capital breeding elephant seals

Recruitment age plays a key role in life-history evolution. Because individuals allocate limited resources among competing life-history functions, theory predicts trade-offs between current reproduction and future growth, survival and/or reproduction. Reproductive costs tend to vary with recruitment age, but may also be overridden by fixed individual differences leading to persistent demographic heterogeneity and positive covariation among demographic traits at the population level. We tested for evidence of intra- and inter-generational trade-offs and individual heterogeneity relating to age at first reproduction using three decades of detailed individual life-history data of 6,439 capital breeding female southern elephant seals. Contrary to the predictions from trade-off hypotheses, we found that recruitment at an early age was associated with higher population level survival and subsequent breeding probabilities. Nonetheless, a survival cost of first reproduction was evident at the population level, as first-time breeders always had lower survival probabilities than prebreeders and experienced breeders of the same age. However, models accounting for hidden persistent demographic heterogeneity revealed that the trade-off between first reproduction and survival was only expressed in “low quality” individuals, comprising 35% of the population. The short-term somatic costs associated with breeding at an early age had no effect on the ability of females to allocate resources to offspring in the next breeding season. Our results provide strong evidence for individual heterogeneity in the life-history trajectories of female elephant seals. By explicitly modeling hidden persistent demographic heterogeneity we show that individual heterogeneity governs the expression of trade-offs with first reproduction in elephant seals.     

Growth and age determination of African savanna elephants

Understanding the population dynamics of savanna elephants depends on estimating population parameters such as the age at first reproduction, calving interval and age-specific survival rates. The generation of these parameters, however, relies on the ability to accurately determine the age of individuals, but a reliable age estimation technique for free-ranging elephants is presently not available. Shoulder heights of elephants were measured in 10 populations in five countries across southern and eastern Africa. Data included shoulder height measurements from two populations where the age of each individual was known (i.e. Addo Elephant National Park, South Africa and Amboseli National Park, Kenya). From the known-age data, Von Bertalanffy growth functions were constructed for both male and female elephants. Savanna elephants were found to attain similar asymptotic shoulder heights in the 10 populations, while individuals in the two known-age populations grew at the same rate. The Von Bertalanffy growth curves allowed for the accurate age estimation of females up to 15 years of age and males up to 36 years of age. The results indicate that shoulder height can serve as an indicator of chronological age for elephants below 15 years of age for females and 36 years of age for males. Ages derived from these growth curves can then be used to generate age-specific population variables, which will help assess the demographic status of savanna elephant populations across Africa.     

Causes and correlates of calf mortality in captive Asian elephants (Elephas maximus)

Juvenile mortality is a key factor influencing population growth rate in density-independent, predation-free, well-managed captive populations. Currently at least a quarter of all Asian elephants live in captivity, but both the wild and captive populations are unsustainable with the present fertility and calf mortality rates. Despite the need for detailed data on calf mortality to manage effectively populations and to minimize the need for capture from the wild, very little is known of the causes and correlates of calf mortality in Asian elephants. Here we use the world''s largest multigenerational demographic dataset on a semi-captive population of Asian elephants compiled from timber camps in Myanmar to investigate the survival of calves (n = 1020) to age five born to captive-born mothers (n = 391) between 1960 and 1999. Mortality risk varied significantly across different ages and was higher for males at any age. Maternal reproductive history was associated with large differences in both stillbirth and liveborn mortality risk: first-time mothers had a higher risk of calf loss as did mothers producing another calf soon (<3.7 years) after a previous birth, and when giving birth at older age. Stillbirth (4%) and pre-weaning mortality (25.6%) were considerably lower than those reported for zoo elephants and used in published population viability analyses. A large proportion of deaths were caused by accidents and lack of maternal milk/calf weakness which both might be partly preventable by supplementary feeding of mothers and calves and work reduction of high-risk mothers. Our results on Myanmar timber elephants with an extensive keeping system provide an important comparison to compromised survivorship reported in zoo elephants. They have implications for improving captive working elephant management systems in range countries and for refining population viability analyses with realistic parameter values in order to predict future population size of the Asian elephant.     

Understanding Long-Term Variations in an Elephant Piosphere Effect to Manage Impacts

Surface water availability is a key driver of elephant impacts on biological diversity. Thus, understanding the spatio-temporal variations of these impacts in relation to water is critical to their management. However, elephant piosphere effects (i.e. the radial pattern of attenuating impact) are poorly described, with few long-term quantitative studies. Our understanding is further confounded by the complexity of systems with elephant (i.e. fenced, multiple water points, seasonal water availability, varying population densities) that likely limit the use of conceptual models to predict these impacts. Using 31 years of data on shrub structure in the succulent thickets of the Addo Elephant National Park, South Africa, we tested elephant effects at a single water point. Shrub structure showed a clear sigmoid response with distance from water, declining at both the upper and lower limits of sampling. Adjacent to water, this decline caused a roughly 300-m radial expansion of the grass-dominated habitats that replace shrub communities. Despite the clear relationship between shrub structure and ecological functioning in thicket, the extent of elephant effects varied between these features with distance from water. Moreover, these patterns co-varied with other confounding variables (e.g. the location of neighboring water points), which limits our ability to predict such effects in the absence of long-term data. We predict that elephant have the ability to cause severe transformation in succulent thicket habitats with abundant water supply and elevated elephant numbers. However, these piosphere effects are complex, suggesting that a more integrated understanding of elephant impacts on ecological heterogeneity may be required before water availability is used as a tool to manage impacts. We caution against the establishment of water points in novel succulent thicket habitats, and advocate a significant reduction in water provisioning at our study site, albeit with greater impacts at each water point.     

Creating Larger and Better Connected Protected Areas Enhances the Persistence of Big Game Species in the Maputaland-Pondoland-Albany Biodiversity Hotspot

The ideal conservation planning approach would enable decision-makers to use population viability analysis to assess the effects of management strategies and threats on all species at the landscape level. However, the lack of high-quality data derived from long-term studies, and uncertainty in model parameters and/or structure, often limit the use of population models to only a few species of conservation concern. We used spatially explicit metapopulation models in conjunction with multi-criteria decision analysis to assess how species-specific threats and management interventions would affect the persistence of African wild dog, black rhino, cheetah, elephant, leopard and lion, under six reserve scenarios, thereby providing the basis for deciding on a best course of conservation action in the South African province of KwaZulu-Natal, which forms the central component of the Maputaland-Pondoland-Albany biodiversity hotspot. Overall, the results suggest that current strategies of managing populations within individual, small, fenced reserves are unlikely to enhance metapopulation persistence should catastrophic events affect populations in the future. Creating larger and better-connected protected areas would ensure that threats can be better mitigated in the future for both African wild dog and leopard, which can disperse naturally, and black rhino, cheetah, elephant, and lion, which are constrained by electric fences but can be managed using translocation. The importance of both size and connectivity should inform endangered megafauna conservation and management, especially in the context of restoration efforts in increasingly human-dominated landscapes.     

Elephants and water provision: what are the management links?

In a recent paper we demonstrated that elephant bull groups and mixed herds exhibited spatial and resource segregation across the Kruger National Park. It was found, inter alia , that both bull groups and mixed herds occurred more frequently closer to rivers than expected if they were randomly distributed, but that only bull groups occurred more frequently closer to the artificial waterholes. Although Chamaillé-Jammes et al. (2007 ) accepted these results, they disagreed with our interpretation regarding the potential effect that closure of artificial waterholes might have. Here we address some of the specific concerns expressed and provide a broader context regarding water provision and elephant management. Although water provision can influence elephant density and distribution, we argue that the effectiveness of surface-water manipulation as a management tool will depend on (1) natural surface-water availability, (2) forage quality, (3) elephant densities, (4) position of a population on its growth trajectory, and (5) management objectives. Even though elephants are water-dependent, the effectiveness of water provision as a management tool will therefore be area- and population-specific and will depend on management objectives.     

The influence of life history milestones and association networks on crop-raiding behavior in male African elephants

Factors that influence learning and the spread of behavior in wild animal populations are important for understanding species responses to changing environments and for species conservation. In populations of wildlife species that come into conflict with humans by raiding cultivated crops, simple models of exposure of individual animals to crops do not entirely explain the prevalence of crop raiding behavior. We investigated the influence of life history milestones using age and association patterns on the probability of being a crop raider among wild free ranging male African elephants; we focused on males because female elephants are not known to raid crops in our study population. We examined several features of an elephant association network; network density, community structure and association based on age similarity since they are known to influence the spread of behaviors in a population. We found that older males were more likely to be raiders than younger males, that males were more likely to be raiders when their closest associates were also raiders, and that males were more likely to be raiders when their second closest associates were raiders older than them. The male association network had sparse associations, a tendency for individuals similar in age and raiding status to associate, and a strong community structure. However, raiders were randomly distributed between communities. These features of the elephant association network may limit the spread of raiding behavior and likely determine the prevalence of raiding behavior in elephant populations. Our results suggest that social learning has a major influence on the acquisition of raiding behavior in younger males whereas life history factors are important drivers of raiding behavior in older males. Further, both life-history and network patterns may influence the acquisition and spread of complex behaviors in animal populations and provide insight on managing human-wildlife conflict.     

Estimating population sizes for elusive animals: the forest elephants of Kakum National Park,Ghana

African forest elephants are difficult to observe in the dense vegetation, and previous studies have relied upon indirect methods to estimate population sizes. Using multilocus genotyping of noninvasively collected samples, we performed a genetic survey of the forest elephant population at Kakum National Park, Ghana. We estimated population size, sex ratio and genetic variability from our data, then combined this information with field observations to divide the population into age groups. Our population size estimate was very close to that obtained using dung counts, the most commonly used indirect method of estimating the population sizes of forest elephant populations. As their habitat is fragmented by expanding human populations, management will be increasingly important to the persistence of forest elephant populations. The data that can be obtained from noninvasively collected samples will help managers plan for the conservation of this keystone species.     

Enriching the captive elephant population genetic pool through artificial insemination with frozen-thawed semen collected in the wild

The first successful AI in an elephant was reported in 1998, using fresh semen. Since then almost 40 calves have been produced through AI in both Asian and African elephants worldwide. Following these successes, with the objective of enriching the captive population with genetic material from the wild, we evaluated the possibility of using frozen-thawed semen collected from wild bulls for AI in captivity. Semen, collected from a 36-yr-old wild African savanna elephant (Loxodonta africana) in South Africa was frozen using the directional freezing technique. This frozen-thawed semen was used for four inseminations over two consecutive days, two before and two after ovulation, in a 26-yr-old female African savanna elephant in Austria. Insemination dose of 1200 × 10⁶ cells per AI with 61% motility resulted in pregnancy, which was confirmed through ultrasound examination 75, 110 and 141 days after the AI procedure. This represents the first successful AI using wild bull frozen-thawed semen in elephants. The incorporation of AI with frozen-thawed semen into the assisted reproduction toolbox opens the way to preserve and transport semen between distant individuals in captivity or, as was done in this study, between wild and captive populations, without the need to transport stressed or potentially disease-carrying animals or to remove animals from the wild. In addition, cryopreserved spermatozoa, in combination with AI, are useful methods to extend the reproductive lifespan of individuals beyond their biological lifespan and an important tool for genetic diversity management and phenotype selection in these endangered mammals.     

Variation in nature: its implications for zoo elephant management

Despite many advances in animal care and welfare over the past few decades, zoos have been criticized recently for the quality of their elephant management programs. More specifically, critics have argued that elephants live miserable lives in captivity and thus should not be kept in zoos. Poor health and reproductive success, they say, are the result of the combined impact of: a lack of exercise; exposure to cold temperatures and disease; and stress due to the use of “brutal” training techniques, chaining and inappropriate social environments. Everyone, including zoo professionals, seems to agree that improvements in zoo elephant management are necessary and appropriate. However, there is considerable disagreement on how to proceed and little information on which to base such decisions. One tactic that the critics have adopted in their efforts to promote change is their frequent reference to “nature” as a yardstick for gauging the adequacy of zoo animal management and care. An argument is made that direct zoo–wild comparisons are of questionable utility and may be invalid from a scientific perspective. Some critics talk about “nature” as if it represented a fixed set of rules by which captive managers must either abide by or risk diminishing the health and welfare of their charges. However, many aspects of elephant natural history vary greatly depending on prevailing environmental conditions and elephants may be much more flexible than many critics are giving them credit for. Thus, although zoo animal managers should look to nature for clues about how to best care for captive elephants, they should not feel constrained by them. This revelation is not intended as an excuse for poor elephant management or to support the status quo. On the contrary, a better approach is to develop realistic and biologically meaningful metrics that reflect the quality of elephant care and welfare and to use them to measure the success of evolving zoo elephant programs. Zoo Biol 25:161–171, 2006. © 2006 Wiley‐Liss, Inc.     

Freezing African Elephant Semen as a New Population Management Tool

Background

The captive elephant population is not self-sustaining and with a limited number of breeding bulls, its genetic diversity is in decline. One way to overcome this is to import young and healthy animals from the wild. We introduce here a more sustainable alternative method - importation of semen from wild bulls without removing them from their natural habitat. Due to the logistics involved, the only practical option would be to transport cryopreserved sperm. Despite some early reports on African elephant semen cryopreservation, the utility of this new population management tool has not been evaluated.

Methodology/Principal Findings

Semen was collected by electroejaculation from 14 wild African savanna elephant (Loxodonta africana) bulls and cryopreserved using the directional freezing technique. Sperm treatments evaluated included the need for centrifugation, the use of hen or quail yolk, the concentration of glycerol (3%, 5% or 7%) in the extender, and maintenance of motility over time after thawing. Our results suggest that dilution in an extender containing hen yolk and 7% glycerol after centrifugation best preserved post-thaw sperm motility when compared to all other treatments (P≤0.012 for all). Using this approach we were able to achieve after thawing (mean ± SD) 54.6±3.9% motility, 85.3±2.4% acrosome integrity, and 86.8±4.6% normal morphology with no decrease in motility over 1 h incubation at 37°C. Sperm cryopreserved during this study has already lead to a pregnancy of a captive female elephant following artificial insemination.

Conclusions/Significance

With working techniques for artificial insemination and sperm cryopreservation of both African and Asian elephants in hand, population managers can now enrich captive or isolated wild elephant populations without removing valuable individuals from their natural habitat.     

Whisker growth in wild Eurasian badgers Meles meles: implications for stable isotope and bait marking studies

The use of biomarkers such as stable isotopes to study the foraging ecology and movement of animals is a rapidly expanding area of research. With respect to mammals, the analysis of inert keratinous tissue such as whiskers (vibrissae) is particularly attractive as they can be sequentially sampled to provide a long-term time series of individual movement or diet. However, in order to interpret data from such tissues researchers require details of growth rates and patterns, and also how these vary within populations. In this study, we use the fluorescent biomarker Rhodamine B to measure vibrissa growth rate and patterns in a wild population of Eurasian badgers. In addition, we compare stable isotope ratio values of blood and vibrissae in order to test whether vibrissae are retained for long periods following growth. We found that badger vibrissae grow at an average rate of 0.43 mm?day^?1 (range 0.23–0.83) such that single vibrissae sampled for stable isotope analysis contain an average of 104 days of ecological data. Age, sex and body condition did not affect growth rate, and there was no evidence of consistent individual differences in growth rate or long-term retention of vibrissae following growth. However, variation in growth rate within the population suggest that the temporal scales reflected in vibrissae may vary both between and within individuals, such that results are not always directly, temporally comparable. This research provides useful information for any future research using vibrissae in combination with biomarkers to study mammalian ecology.