Asian elephant calf physiology and mahout perspectives during taming in Myanmar.

A quarter of Asian elephants are captive, with greater than 90% of these tamed and cared for by handlers (mahouts) in Asia. Although taming is a much-discussed welfare issue, no studies to our knowledge have empirically assessed its impact on calves, and dialogue surrounding taming often lacks perspectives of those involved. Here, we interviewed mahouts involved in taming and monitored five physiological measures (faecal glucocorticoid metabolites (FGMs), serum cortisol, glucose, creatine kinase (CK) and heterophil:lymphocyte (H:L)) over the first 10 days of taming and following six months in 41 calves undergoing taming and 16 control individuals. These measures assess the duration and intensity of stress during taming. Interviews suggested mahouts had major concerns for their safety when discussing changing taming practices, an important consideration for future management. Calf physiological measures were elevated by 50-70% (FGMs/cortisol/glucose), 135% (H:L) and greater than 500% (CK) over the first few days of taming, indicative of elevated stress, not seen to the same extent in control adults. Some measures stabilized sooner (glucose/cortisol/CK/FGM: 7-10 days) than others (H:L: one-two months), indicating mostly acute stress. Our findings inform the welfare of approximately 15 000 captive elephants around the world. Future studies should compare taming in different populations and consider calf and mahout welfare.

Seasonal variation in molecular and physiological stress markers in Asian elephants.

Free-living species exhibit seasonal variation in various life history traits, including vital rates such as birth and death patterns. Different physiological mechanisms are thought to underlie the expression of life history traits that contribute to lifetime fitness. However, although the broad impacts of seasonality on life history traits and trade-offs is well established in many systems, the exact physiological mechanisms responsible for driving differences within and between individuals are poorly understood. Among them, molecular and physiological stress pathways, such as stress hypothalamic-pituitary-adrenal axis and oxidative stress, have potential to mediate relationships between individual survival, reproduction and environmental seasonality. Here, we determine how different physiological markers of stress including faecal cortisol metabolites (FCMs), heterophils/lymphocytes (H/L) ratio, two markers indicating oxidative balance including a marker of oxidative damage (reactive oxygen metabolites, ROM) and a marker of antioxidant defences (superoxide dismutase, SOD) and body weight vary in a large semi-captive population of Asian elephants (Elephas maximus) exposed to extreme seasonality (e.g. elevated temperatures). Individuals showed higher FCM levels and H/L ratios during cold season, indicating increased stress, and the lowest FCM levels during monsoon season and H/L ratios during hot and dry season, but we found no pattern in oxidative stress (ROM and SOD) levels. Hot season also associated with a decline in body weight. The present study shows how different physiological parameters (FCM levels and H/L ratio), molecular (oxidative stress) and body condition vary with seasonal changes, and how these parameters might allow individuals to adapt to such variations. Our results on an endangered long-lived species are crucial in indicating the most productive timing for conservation efforts, predicting how individuals cope with environmental changes, and allow for a more accurate representation of how animal physiology operates in nature.

Investigating associations between nematode infection and three measures of sociality in Asian elephants.

Abstract: Frequent social interactions, proximity to conspecifics, and group density are main drivers of infections and parasite transmissions. However, recent theoretical and empirical studies suggest that the health benefits of sociality and group living can outweigh the costs of infection and help social individuals fight infections or increase their infection-related tolerance level. Here, we combine the advantage of studying artificially created social work groups with different demographic compositions with free-range feeding and social behaviours in semi-captive Asian elephants (Elephas maximus), employed in timber logging in Myanmar. We examine the link between gastro-intestinal nematode load (strongyles and Strongyloides spp.), estimated by faecal egg counts, and three different aspects of an elephant's social world: individual solitary behaviour, work group size, and work group sex ratio. Controlling for sex, age, origin, time since last deworming treatment, year, human sampler bias, and individual identity, we found that infection by nematodes ranged from 0 to 2720 eggs/g between and within 26 male and 45 female elephants over the 4-year study period. However, such variation was not linked to any investigated measures of sociality in either males or females. Our findings highlight the need for finer-scale studies, establishing how sociality is limited by, mitigates, or protects against infection in different ecological contexts, to fully understand the mechanisms underlying these pathways. Significance statement: Being social involves not only benefits, such as improved health, but also costs, including increased risk of parasitism and infectious disease. We studied the relationship between and three different sociality measures-solitary behaviour, group size, and the proportion of females to males within a group-and infection by gut nematodes (roundworms), using a unique study system of semi-captive working Asian elephants. Our system allows for observing how infection is linked to sociality measures across different social frameworks. We found that none of our social measures was associated with nematode infection in the studied elephants. Our results therefore suggest that here infection is not a large cost to group living, that it can be alleviated by the benefits of increased sociality, or that there are weak infection-sociality associations present which could not be captured and thus require finer-scale measures than those studied here. Overall, more studies are needed from a diverse range of systems that investigate specific aspects of social infection dynamics. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-022-03192-8.

Sex-specific body mass ageing trajectories in adult Asian elephants.

In species with marked sexual dimorphism, the classic prediction is that the sex which undergoes stronger intrasexual competition ages earlier or quicker. However, more recently, alternative hypotheses have been put forward, showing that this association can be disrupted. Here, we utilize a unique, longitudinal data set of a semi-captive population of Asian elephants (Elephas maximus), a species with marked male-biased intrasexual competition, with males being larger and having shorter lifespans, and investigate whether males show earlier and/or faster body mass ageing than females. We found evidence of sex-specific body mass ageing trajectories: adult males gained weight up to the age of 48 years old, followed by a decrease in body mass until natural death. In contrast, adult females gained body mass with age until a body mass decline in the last year of life. Our study shows sex-specific ageing patterns, with an earlier onset of body mass declines in males than females, which is consistent with the predictions of the classical theory of ageing.

Sex-specific links between the social landscape and faecal glucocorticoid metabolites in semi-captive Asian elephants.

Although social behaviour is common in group-living mammals, our understanding of its mechanisms in long-lived animals is largely based on studies in human and non-human primates. There are health and fitness benefits associated with strong social ties, including increased life span, reproductive success, and lower disease risk, which are attributed to the proximate effects of lowered circulating glucocorticoid hormones. However, to deepen our understanding of health-social dynamics, we must explore species beyond the primate order. Here, using Asian elephants as a model species, we combine social data generated from semi-captive timber elephants in Myanmar with measurements of faecal glucocorticoid metabolite (FGM) concentrations. These data enable a "natural experiment" because individuals live in work groups with different demographic compositions. We examine sex-specific FGM concentrations for four different aspects of an individuals' social world: general sociality, work group size, sex ratio and the presence of immatures (<5 years) within the work group. Males experienced lower FGM concentrations when engaged in more social behaviours and residing in female-biased work groups. Surprisingly, females only exhibited lower FGM concentrations when residing with calves. Together, our findings highlight the importance of sociality on individual physiological function among elephants, which may have broad implications for the benefits of social interactions among mammals.

Age related variation of health markers in Asian elephants.

Although senescence is often observed in the wild, its underlying mechanistic causes can rarely be studied alongside its consequences, because data on health, molecular and physiological measures of senescence are rare. Documenting how different age-related changes in health accelerate ageing at a mechanistic level is key if we are to better understand the ageing process. Nevertheless, very few studies, particularly on natural populations of long-lived animals, have investigated age-related variation in biological markers of health and sex differences therein. Using blood samples collected from semi-captive Asian elephants, we show that pronounced differences in haematology, blood chemistry, immune, and liver functions among age classes are also evident under natural conditions in this extremely long-lived mammal. We provide strong support that overall health declined with age, with progressive declines in immune and liver functions similarly in both males and females. These changes parallel those mainly observed to-date in humans and laboratory mammals, and suggest a certain ubiquity in the ageing patterns.

The elephant in the family: Costs and benefits of elder siblings on younger offspring life-history trajectory in a matrilineal mammal.

Many mammals grow up with siblings, and interactions between them can influence offspring phenotype and fitness. Among these interactions, sibling competition between different-age offspring should lead to reproductive and survival costs on the younger sibling, while sibling cooperation should improve younger sibling's reproductive potential and survival. However, little is known about the consequences of sibling effects on younger offspring life-history trajectory, especially in long-lived mammals. We take advantage of a large, multigenerational demographic dataset from semi-captive Asian elephants to investigate how the presence and sex of elder siblings influence the sex, survival until 5 years old, body condition, reproductive success (i.e. age at first reproduction and lifetime reproductive success) and long-term survival of subsequent offspring. We find that elder siblings have heterogeneous effects on subsequent offspring life-history traits depending on their presence, their sex and the sex of the subsequent offspring (named focal calf). Overall, the presence of an elder sibling (either sex) strongly increased focal calf long-term survival (either sex) compared to sibling absence. However, elder sisters had higher impact on the focal sibling than elder brothers. Focal females born after a female display higher long-term survival, and decreased age at first reproduction when raised together with an elder sister rather than a brother. Focal males born after a female rather than a male showed lower survival but higher body weight when both were raised together. We did not detect any sibling effects on the sex of the focal calf sex, survival until 5 years old and lifetime reproductive success. Our results highlight the general complexity of sibling effects, but broadly that elder siblings can influence the life-history trajectory of subsequent offspring. We also stress the importance of considering all life stages when evaluating sibling effects on life trajectories.

Denombreux mammifères grandissent en fratrie, et les interactions au sein de lafratrie peuvent influencer le phénotype et la valeur sélective des jeunes.Parmi ces interactions, la compétition entre frères et sœurs d'âges différentspeut entraîner des coûts de reproduction et de survie pour le/la plus jeune,tandis que les interactions coopératives améliorent la reproduction et lasurvie du/de la plus jeune. Cependant, nous avons encore peu de connaissancessur l'influence de la fratrie sur la trajectoire de vie des frères et sœursplus jeunes, en particulier chez les mammifères longévifs. Grâce àun jeu de données démographique multigénérationnel d'éléphants d'Asiesemi-captifs, nous avons pu étudier comment la présence d'un frère aînéou d'une sœur aînée influence le sexe, la survie jusqu'à l'âge de cinqans, la masse corporelle, la reproduction (i.e. l'âge de première reproductionet le succès reproductif sur toute la vie) et la survie à long terme du jeunesuivant. Nousobservons que les frères et sœurs aînés ont des effets hétérogènes sur lestraits d'histoire de vie du jeune suivant et ce, en fonction de leur présence,et du sexe du jeune suivant (appelé focal). Dansl'ensemble, la présence d'un frère aîné oud'une sœur aînée augmente fortement la survie à long terme du jeune focal parrapport à leur absence. Cependant, il est à noter que les sœurs aînées ont unimpact plus important que les frères ainés sur le frère focal. Les femellesfocales présentent une survie à long terme plus élevée et un âge de premièrereproduction plus précoce lorsqu'elles sont élevées avec une sœur aînée plutôtqu'un frère. Les mâles focaux élevés avec une grande sœur plutôt qu'un grandfrère présentent une survie plus faible mais un poids corporel plus élevé. Nousn'avons détecté aucun effet des frères aînés ou sœurs aînées sur le sexe, la survie jusqu'àl'âge de cinq ans et le succès reproducteur sur toute la vie du jeune focal. Nosrésultats mettent en évidence la complexité des effets de la fratrie et, lefait que les frères et sœurs plus âgés peuvent influencer la trajectoire ducycle de vie des jeunes suivant. Nous soulignons également l'importance deconsidérer toutes les étapes de la vie lors de l'évaluation des effets de lafratrie sur les trajectoires de vie.

Handler familiarity helps to improve working performance during novel situations in semi-captive Asian elephants.

Working animals spend hours each day in close contact with humans and require training to understand commands and fulfil specific tasks. However, factors driving cooperation between humans and animals are still unclear, and novel situations may present challenges that have been little-studied to-date. We investigated factors driving cooperation between humans and animals in a working context through behavioural experiments with 52 working semi-captive Asian elephants. Human-managed Asian elephants constitute approximately a third of the remaining Asian elephants in the world, the majority of which live in their range countries working alongside traditional handlers. We investigated how the familiarity and experience of the handler as well as the elephant's age and sex affected their responses when asked to perform a basic task and to cross a novel surface. The results highlighted that when novelty is involved in a working context, an elephant's relationship length with their handler can affect their cooperation: elephants who had worked with their handler for over a year were more willing to cross the novel surface than those who had a shorter relationship with their handler. Older animals also tended to refuse to walk on the novel surface more but the sex did not affect their responses. Our study contributes much needed knowledge on human-working animal relationships which should be considered when adjusting training methods and working habits.

Demographic and reproductive associations with nematode infection in a long-lived mammal.

Infection by macroparasites, such as nematodes, varies within vertebrate host systems; elevated infection is commonly observed in juveniles and males, and, for females, with different reproductive states. However, while such patterns are widely recognized in short-lived model systems, how they apply to long-lived hosts is comparatively understudied. Here, we investigated how infection varies with host age, sex, and female reproduction in a semi-captive population of individually marked Asian elephants Elephas maximus. We carried out 1,977 faecal egg counts (FECs) across five years to estimate nematode loads for 324 hosts. Infection patterns followed an established age-infection curve, whereby calves (5 years) exhibited the highest FECs and adults (45 years) the lowest. However, males and females had similar FECs across their long lifespan, despite distinct differences in life-history strategy and clear sexual dimorphism. Additionally, although mothers invest two years in pregnancy and a further three to five years into lactation, nematode load did not vary with four different measures of female reproduction. Our results provide a much-needed insight into the host-parasite dynamics of a long-lived host; determining host-specific associations with infection in such systems is important for broadening our knowledge of parasite ecology and provides practical applications for wildlife medicine and management.

Changes in age-structure over four decades were a key determinant of population growth rate in a long-lived mammal.

A changing environment directly influences birth and mortality rates, and thus population growth rates. However, population growth rates in the short term are also influenced by population age-structure. Despite its importance, the contribution of age-structure to population growth rates has rarely been explored empirically in wildlife populations with long-term demographic data. Here we assessed how changes in age-structure influenced short-term population dynamics in a semi-captive population of Asian elephants Elephas maximus. We addressed this question using a demographic dataset of female Asian elephants from timber camps in Myanmar spanning 45 years (1970-2014). First, we explored temporal variation in age-structure. Then, using annual matrix population models, we used a retrospective approach to assess the contributions of age-structure and vital rates to short-term population growth rates with respect to the average environment. Age-structure was highly variable over the study period, with large proportions of juveniles in the years 1970 and 1985, and made a substantial contribution to annual population growth rate deviations. High adult birth rates between 1970 and 1980 would have resulted in large positive population growth rates, but these were prevented by a low proportion of reproductive-aged females. We highlight that an understanding of both age-specific vital rates and age-structure is needed to assess short-term population dynamics. Furthermore, this example from a human-managed system suggests that the importance of age-structure may be accentuated in populations experiencing human disturbance where age-structure is unstable, such as those in captivity or for endangered species. Ultimately, changes to the environment drive population dynamics by influencing birth and mortality rates, but understanding demographic structure is crucial for assessing population growth.

Taming age mortality in semi-captive Asian elephants.

Understanding factors preventing populations of endangered species from being self-sustaining is vital for successful conservation, but we often lack sufficient data to understand dynamics. The global Asian elephant population has halved since the 1950s, however >25% currently live in captivity and effective management is essential to maintain viable populations. Here, we study the largest semi-captive Asian elephant population, those of the Myanma timber industry (~20% global captive population), whose population growth is heavily limited by juvenile mortality. We assess factors associated with increased mortality of calves aged 4.0-5.5 years, the taming age in Myanmar, a process affecting ~15,000 captive elephants to varying degrees worldwide. Using longitudinal survival data of 1,947 taming-aged calves spanning 43 years, we showed that calf mortality risk increased by >50% at the taming age of four, a peak not seen in previous studies on wild African elephants. Calves tamed at younger ages experienced higher mortality risk, as did calves with less experienced mothers. Taming-age survival greatly improved after 2000, tripling since the 1970's. Management should focus on reducing risks faced by vulnerable individuals such as young and first-born calves to further improve survival. Changes associated with reduced mortality here are important targets for improving the sustainability of captive populations.

Evaluating the Reliability of Non-Specialist Observers in the Behavioural Assessment of Semi-Captive Asian Elephant Welfare.

Recognising stress is an important component in maintaining the welfare of captive animal populations, and behavioural observation provides a rapid and non-invasive method to do this. Despite substantial testing in zoo elephants, there has been relatively little interest in the application of behavioural assessments to the much larger working populations of Asian elephants across Southeast Asia, which are managed by workers possessing a broad range of behavioural knowledge. Here, we developed a new ethogram of potential stress- and work-related behaviour for a semi-captive population of Asian elephants. We then used this to collect observations from video footage of over 100 elephants and evaluated the reliability of behavioural welfare assessments carried out by non-specialist observers. From observations carried out by different raters with no prior experience of elephant research or management, we tested the reliability of observations between-observers, to assess the general inter-observer agreement, and within-observers, to assess the consistency in behaviour identification. The majority of ethogram behaviours were highly reliable both between- and within-observers, suggesting that overall, behaviour was highly objective and could represent easily recognisable markers for behavioural assessments. Finally, we analysed the repeatability of individual elephant behaviour across behavioural contexts, demonstrating the importance of incorporating a personality element in welfare assessments. Our findings highlight the potential of non-expert observers to contribute to the reliable monitoring of Asian elephant welfare across large captive working populations, which may help to both improve elephant wellbeing and safeguard human workers.

Faecal Glucocorticoid Metabolites and H/L Ratio are Related Markers of Stress in Semi-Captive Asian Timber Elephants.

Animals are kept in captivity for various reasons, but species with a slower pace of life may adapt to captive environments less easily, leading to welfare concerns and the need to assess stress reliably in order to develop effective interventions. Our aim was to assess welfare of semi-captive timber elephants from Myanmar by investigating the relationship between two physiological markers of stress commonly used as proxies for welfare, faecal glucocorticoid metabolite concentrations (FGM) and heterophil/lymphocyte ratios (H/L), and link these measures to changes in body condition (determined by body weight). We further assessed how robustly these two markers of stress performed in animals of different age or sex, or in different ecological contexts. We measured FGM concentrations and H/L ratios between 2016 and 2018 from 316 samples of 75 females and 49 males ranging in age from 4 to 68. We found a positive and consistent link between FGMs and H/L ratios in Asian elephants, irrespective of their sex, age, or ecological context. Our results will help to inform managers of (semi-) captive elephants about using heterophil/lymphocyte ratio data from blood smears on site as a potentially cheaper and faster alternative to determining stress than measuring faecal glucocorticoid metabolite concentrations in the laboratory.

Seasonal variation of health in Asian elephants.

Long-lived species are often predicted to be buffered against seasonal variation: longevity means low annual mortality and reproductive rates and annual variability in climate may therefore have a smaller impact on population growth rates of long-lived species in comparison to short-lived ones. However, little is known of the physiological mechanisms underlying such patterns in long-lived species. In this study, we investigated seasonal variation in the health of Asian elephants living in a seasonal monsoon climate. We used two complementary methods: (i) global and (ii) trait-by-trait analyses of seasonal effects on 23 health parameters of 225 individually marked elephants with known age and reproductive and health history, with repeated measures per individual over a 26-month period. The global analysis highlighted the biggest differences in health between the hot and monsoon seasons. Our trait-specific analyses identified the physiological functions underlying such health variation in different ecological settings, including haematological, immunological, muscular, kidney and liver functions, as well as protein balance and electrolytes. Overall, the results suggest that even long-lived, large mammals may experience physiological changes in response to seasonal variation that in extreme circumstances can pose a significant health risk.

Maternal age at birth shapes offspring life-history trajectory across generations in long-lived Asian elephants.

Advanced maternal age at birth can have pronounced consequences for offspring health, survival and reproduction. If carried over to the next generation, such fitness effects could have important implications for population dynamics and the evolution of ageing, but these remain poorly understood. While many laboratory studies have investigated maternal age effects, relatively few studies have been conducted in natural populations, and they usually only present a "snapshot" of an offspring's lifetime. In the present study, we focus on how maternal age influences offspring life-history trajectories and performance in a long-lived mammal. We use a multigenerational demographic dataset of semi-captive Asian elephants to investigate maternal age effects on several offspring life-history traits: condition, reproductive success and overall survival. We show that offspring born to older mothers display reduced overall survival but higher reproductive success, and reduced survival of their own progeny. Our results show evidence of a persistent effect of maternal age on fitness across generations in a long-lived mammal. By highlighting transgenerational effects on the fitness of the next generation associated with maternal age, the present study helps increase our understanding of factors contributing to individual variation in ageing rates and fitness.

Asian elephants exhibit post-reproductive lifespans.

BACKGROUND: The existence of extended post-reproductive lifespan is an evolutionary puzzle, and its taxonomic prevalence is debated. One way of measuring post-reproductive life is with post-reproductive representation, the proportion of adult years lived by females after cessation of reproduction. Analyses of post-reproductive representation in mammals have claimed that only humans and some toothed whale species exhibit extended post-reproductive life, but there are suggestions of a post-reproductive stage for false killer whales and Asian elephants. Here, we investigate the presence of post-reproductive lifespan in Asian elephants using an extended demographic dataset collected from semi-captive timber elephants in Myanmar. Furthermore, we investigate the sensitivity of post-reproductive representation values to availability of long-term data over 50 years. RESULTS: We find support for the presence of an extended post-reproductive stage in Asian elephants, and that post-reproductive representation and its underlying demographic rates depend on the length of study period in a long-lived animal. CONCLUSIONS: The extended post-reproductive lifespan is unlikely due to physiological reproductive cessation, and may instead be driven by mating preferences or condition-dependent fertility. Our results also show that it is crucial to revisit such population measures in long-lived species as more data is collected, and if the typical lifespan of the species exceeds the initial study period.

Capture from the wild has long-term costs on reproductive success in Asian elephants.

Capturing wild animals is common for conservation, economic or research purposes. Understanding how capture itself affects lifetime fitness measures is often difficult because wild and captive populations live in very different environments and there is a need for long-term life-history data. Here, we show how wild capture influences reproduction in 2685 female Asian elephants (Elephas maximus) used in the timber industry in Myanmar. Wild-caught females demonstrated a consistent reduction in breeding success relative to captive-born females, with significantly lower lifetime reproduction probabilities, lower breeding probabilities at peak reproductive ages and a later age of first reproduction. Furthermore, these negative effects lasted for over a decade, and there was a significant influence on the next generation: wild-caught females had calves with reduced survival to age 5. Our results suggest that wild capture has long-term consequences for reproduction, which is important not only for elephants, but also for other species in captivity.

Evolutionary significance of maternal kinship in a long-lived mammal.

Preferential treatment of kin is widespread across social species and is considered a central prerequisite to the evolution of cooperation through kin selection. Though it is well known that, among most social mammals, females will remain within their natal group and often bias social behaviour towards female maternal kin, less is known about the fitness consequences of these relationships. We test the fitness benefits of living with maternal sisters, measured by age-specific female reproduction, using an unusually large database of a semi-captive Asian elephant ( Elephas maximus) population. This study system is particularly valuable to an exploration of reproductive trends in a long-lived mammal, because it includes life-history data that span multiple generations, enabling a study of the effects of kinship across a female's lifespan. We find that living near a sister significantly increased the likelihood of annual reproduction among young female elephants, and this effect was strongest when living near a sister 0-5 years younger. Our results show that fitness benefits gained from relationships with kin are age-specific, establish the basis necessary for the formation and maintenance of close social relationships with female kin, and highlight the adaptive importance of matriliny in a long-lived mammal. This article is part of the theme issue 'The evolution of female-biased kinship in humans and other mammals'.

Long-term trends in wild-capture and population dynamics point to an uncertain future for captive elephants.

Maintaining sustainable populations in captivity without supplementation through wild-capture is a major challenge in conservation that zoos and aquaria are working towards. However, the capture of wild animals continues for many purposes where conservation is not the primary focus. Wild-capture hinders long-term conservation goals by reducing remaining wild populations, but the direct and long-term indirect consequences of wild-capture for captive population viability are rarely addressed using longitudinal data. We explored the implications of changes in wild-capture on population dynamics in captivity over 54 years using a multi-generational studbook of working Asian elephants ( Elephas maximus) from Myanmar, the largest remaining captive elephant population. Here we show that population growth and birth rates declined between 1960 and 2014 with declines in wild-capture. Importantly, wild-caught females had reduced birth rates and a higher mortality risk. However, despite the disadvantages of wild-capture, the population may not be sustainable without it, with immediate declines owing to an unstable age-structure that may last for 50 years. Our results highlight the need to assess the long-term demographic consequences of wild-capture to ensure the sustainability of captive and wild populations as species are increasingly managed and conserved in altered or novel environments.