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.     

Elephant Genomes Reveal Accelerated Evolution in Mechanisms Underlying Disease Defenses

Disease susceptibility and resistance are important factors for the conservation of endangered species, including elephants. We analyzed pathology data from 26 zoos and report that Asian elephants have increased neoplasia and malignancy prevalence compared with African bush elephants. This is consistent with observed higher susceptibility to tuberculosis and elephant endotheliotropic herpesvirus (EEHV) in Asian elephants. To investigate genetic mechanisms underlying disease resistance, including differential responses between species, among other elephant traits, we sequenced multiple elephant genomes. We report a draft assembly for an Asian elephant, and defined 862 and 1,017 conserved potential regulatory elements in Asian and African bush elephants, respectively. In the genomes of both elephant species, conserved elements were significantly enriched with genes differentially expressed between the species. In Asian elephants, these putative regulatory regions were involved in immunity pathways including tumor-necrosis factor, which plays an important role in EEHV response. Genomic sequences of African bush, forest, and Asian elephant genomes revealed extensive sequence conservation at TP53 retrogene loci across three species, which may be related to TP53 functionality in elephant cancer resistance. Positive selection scans revealed outlier genes related to additional elephant traits. Our study suggests that gene regulation plays an important role in the differential inflammatory response of Asian and African elephants, leading to increased infectious disease and cancer susceptibility in Asian elephants. These genomic discoveries can inform future functional and translational studies aimed at identifying effective treatment approaches for ill elephants, which may improve conservation.     

Endocrine Correlates of Musth in Free-Ranging Asian Elephants (Elephas maximus) Determined by Non-Invasive Faecal Steroid Hormone Metabolite Measurements

The occurrence of musth, a period of elevated levels of androgens and heightened sexual activity, has been well documented for the male Asian elephant (Elephas maximus). However, the relationship between androgen-dependent musth and adrenocortical function in this species is unclear. The current study is the first assessment of testicular and adrenocortical function in free-ranging male Asian elephants by measuring levels of testosterone (androgen) and cortisol (glucocorticoid – a physiological indicator of stress) metabolites in faeces. During musth, males expectedly showed significant elevation in faecal testosterone metabolite levels. Interestingly, glucocorticoid metabolite concentrations remained unchanged between musth and non-musth periods. This observation is contrary to that observed with wild and captive African elephant bulls and captive Asian bull elephants. Our results show that musth may not necessarily represent a stressful condition in free-ranging male Asian elephants.     

Sexual Dimorphism and Inter-Generic Variation in Proboscidean Tusks: Multivariate Assessment of American Mastodons (Mammut americanum) and Extant African Elephants

Characteristics of social structure, mating strategies, and parental investment can be inferred for mammalian species based on degree of sexual dimorphism, especially when males are substantially larger than females. American mastodons (Mammut americanum) and extant African elephants (Loxodonta africana, Loxodonta cyclotis) both exhibit marked dimorphism in tusk size. To evaluate the hypothesis that this dimorphism might be indicative of similar, and possibly conserved, behavioral patterns in each lineage, we undertook a detailed evaluation of the pattern of tusk growth in these two genera. Separate discriminant function analyses (DFA) of 21 adult mastodon tusks of inferred sex and 48 adult elephant tusks of known sex show that patterns of ontogenetic change in tusk circumference, regardless of genus, effectively discriminate between sexes. Canonical variates analysis (CVA) of tusks from male and female mastodons and male and female elephants shows that male tusks in both genera are larger than female tusks across all measurements, especially for maximum tusk circumference and pulp cavity depth. CVA’s emphasis of inter-group differences in tusk morphology also shows that mastodon tusks are more robust than elephant tusks. Overall, this study illustrates that there is a characteristic male and a characteristic female tusk form shared by elephants and mastodons. This shows that elephants and mastodons display a shared syndrome of traits beyond sex-linked differences in tusk size, supporting the hypothesis that mastodons exhibited behaviors similar to those we observe today in African elephants.     

Epigenetic clock and methylation studies in elephants

Age‐associated DNA‐methylation profiles have been used successfully to develop highly accurate biomarkers of age ("epigenetic clocks") in humans, mice, dogs, and other species. Here we present epigenetic clocks for African and Asian elephants. These clocks were developed using novel DNA methylation profiles of 140 elephant blood samples of known age, at loci that are highly conserved between mammalian species, using a custom Infinium array (HorvathMammalMethylChip40). We present epigenetic clocks for Asian elephants (Elephas maximus), African elephants (Loxodonta africana), and both elephant species combined. Two additional human‐elephant clocks were constructed by combining human and elephant samples. Epigenome‐wide association studies identified elephant age‐related CpGs and their proximal genes. The products of these genes play important roles in cellular differentiation, organismal development, metabolism, and circadian rhythms. Intracellular events observed to change with age included the methylation of bivalent chromatin domains, and targets of polycomb repressive complexes. These readily available epigenetic clocks can be used for elephant conservation efforts where accurate estimates of age are needed to predict demographic trends.     

Genomic DNA sequences from mastodon and woolly mammoth reveal deep speciation of forest and savanna elephants

To elucidate the history of living and extinct elephantids, we generated 39,763 bp of aligned nuclear DNA sequence across 375 loci for African savanna elephant, African forest elephant, Asian elephant, the extinct American mastodon, and the woolly mammoth. Our data establish that the Asian elephant is the closest living relative of the extinct mammoth in the nuclear genome, extending previous findings from mitochondrial DNA analyses. We also find that savanna and forest elephants, which some have argued are the same species, are as or more divergent in the nuclear genome as mammoths and Asian elephants, which are considered to be distinct genera, thus resolving a long-standing debate about the appropriate taxonomic classification of the African elephants. Finally, we document a much larger effective population size in forest elephants compared with the other elephantid taxa, likely reflecting species differences in ancient geographic structure and range and differences in life history traits such as variance in male reproductive success.     

Secretory Pattern of Inhibin During Estrous Cycle and Pregnancy in African (Loxodonta africana) and Asian (Elephas maximus) Elephants

The ovary of female elephants has multiple corpora lutea (CL) during the estrous cycle and gestation. The previous reports clearly demonstrated that inhibin was secreted from lutein cells as well as granulosa cells of antral follicles in cyclic Asian elephants. The aim of this study is to investigate the inhibin secretion during the pregnancy in African and Asian elephants. Two African elephants and two Asian elephants were subjected to this study. Circulating levels of immunoreactive (ir‐) inhibin and progesterone were measured by radioimmunoassay. Four pregnant periods of an African elephant and three pregnant periods of an Asian elephant were analyzed in this study. Circulating levels of ir‐inhibin started to increase at 1 or 2 week before the ovulation and reached the peak level 3 or 4 weeks earlier than progesterone during the estrous cycle in both African and Asian elephants. After last luteal phase, the serum levels of ir‐inhibin remained low throughout pregnancy in both an African and an Asian elephant. The mean levels of ir‐inhibin during the pregnancy were lower than the luteal phase in the estrous cycle despite high progesterone levels were maintained throughout the pregnancy. These results strongly suggest that CL secrete a large amount of progesterone but not inhibin during the pregnancy in elephants. Zoo Biol 31:511‐522, 2012. © 2011 Wiley Periodicals, Inc.     

Observations on the length of the intestinal tract of African <Emphasis Type="Italic">Loxodonta africana</Emphasis> (Blumenbach 1797) and Asian elephants <Emphasis Type="Italic">Elephas maximus</Emphasis> (Linné 1735)

The digestive tract of elephants is surprisingly short compared to other herbivorous mammals. However, measurements relating the length of the intestine to the body mass of the respective individual are rare. In this study, we report such data for an African elephant and an Asian elephant. Our data support the hypothesis that Asian elephants have a longer intestinal tract than their African counterparts. These findings are in accord with the observation of longer retention times and higher digestion coefficients in Asian as compared to African elephants. This difference between the species could be the reflection of slightly different ecological niches, with Asian elephants adapted to a natural diet with a higher proportion of grass.     

Ovarian function in the elephant: luteinizing hormone and progesterone cycles in African and Asian elephants

Serum samples were collected weekly for 3 yr from two female African elephants, for 18 mo from two other female African elephants, and for 2 yr from two female Asian elephants. Animals were not sedated at the time of blood collection. Ovarian cycles, characterized by changes in progesterone and immunoreactive luteinizing hormone (ILH) concentrations, averaged 15.9 +/- 0.6 wk (N = 25) for African females and 14.7 +/- 0.5 wk for Asian females (N = 10). The length of the active luteal phase averaged 10.0 +/- 0.3 wk for African elephants (range 8-14 wk) and 10.6 +/- 0.6 wk for Asian females (range 9-13 wk). Interluteal phases were 5.9 +/- 0.6 wk for African females and 4.2 +/- 0.5 wk for Asian females. One African female (Maliaca) had two extended interluteal phases, both occurring between the months of February and May. Excluding these two periods, there were no differences in the length of the ovarian cycle or the length of the luteal phase between species of elephant. Serum progesterone in both species ranged from less than 50 pg/ml to 933 pg/ml. Average progesterone concentrations during the luteal phase were significantly lower in African elephants compared with Asian elephants (328 +/- 13, N = 30 cycles vs. 456 +/- 23, N = 14 cycles; p less than 0.001). ILH ranged from nondetectable to 11.6 ng/ml. These data suggest that the length of the ovarian cycle in the African elephant is about 16 wk and confirm that the length of the ovarian cycle in the Asian elephant is about 15 wk.     

Forest Elephants: Tree Planters of the Congo

The abundance of large vertebrates is rapidly declining, particularly in the tropics where over-hunting has left many forests structurally intact but devoid of large animals. An urgent question then, is whether these 'empty' forests can sustain their biodiversity without large vertebrates. Here we examine the role of forest elephant ( Loxodonta africana cyclotis ) seed dispersal in maintaining the community structure of trees in the Ndoki Forest, northern Congo. Analysis of 855 elephant dung piles suggested that forest elephants disperse more intact seeds than any other species or genus of large vertebrate in African forests, while GPS telemetry data showed that forest elephants regularly disperse seeds over unprecedented distances compared to other dispersers. Our analysis of the spatial distribution of trees from a sample of 5667 individuals showed that dispersal mechanism was tightly correlated with the scale of spatial aggregation. Increasing amounts of elephant seed dispersal was associated with decreasing aggregation. At distances of<200 m, trees whose seeds are dispersed only by elephants were less aggregated than the random expectation, suggesting Janzen–Connell effects on seed/seedling mortality. At the landscape scale, seed dispersal mode predicted the rate at which local tree community similarity decayed in space. Our results suggest that the loss of forest elephants (and other large-bodied dispersers) may lead to a wave of recruitment failure among animal-dispersed tree species, and favor regeneration of the species-poor abiotically dispersed guild of trees.     

Long-Term Monitoring of Dzanga Bai Forest Elephants: Forest Clearing Use Patterns

Individual identification of the relatively cryptic forest elephant (Loxodonta cyclotis) at forest clearings currently provides the highest quality monitoring data on this ecologically important but increasingly threatened species. Here we present baseline data from the first 20 years of an individually based study of this species, conducted at the Dzanga Clearing, Central African Republic. A total of 3,128 elephants were identified over the 20-year study (1,244 adults; 675 females, 569 males). It took approximately four years for the majority of elephants visiting the clearing to be identified, but new elephants entered the clearing every year of the study. The study population was relatively stable, varying from 1,668 to 1,864 individuals (including juveniles and infants), with increasingly fewer males than females over time. The age-class distribution for females remained qualitatively unchanged between 1995 and 2010, while the proportion of adult males decreased from 20% to 10%, likely reflecting increased mortality. Visitation patterns by individuals were highly variable, with some elephants visiting monthly while others were ephemeral users with visits separated by multiple years. The number of individuals in the clearing at any time varied between 40 and 100 individuals, and there was little evidence of a seasonal pattern in this variation. The number of elephants entering the clearing together (defined here as a social group) averaged 1.49 (range 1–12) for males and 2.67 (range 1–14) for females. This collation of 20 years of intensive forest elephant monitoring provides the first detailed, long term look at the ecology of bai visitation for this species, offering insight to the ecological significance and motivation for bai use, social behavior, and threats to forest elephants. We discuss likely drivers (rainfall, compression, illegal killing, etc.) influencing bai visitation rates. This study provides the baseline for future demographic and behavioral studies of this population.     

Molecular and morphological evidence on the phylogeny of the Elephantidae

The African and Asian elephants and the mammoth diverged ca. 4-6 million years ago and their phylogenetic relationship has been controversial. Morphological studies have suggested a mammoth Asian elephant relationship, while molecular studies have produced conflicting results. We obtained cytochrome b sequences of up to 545 base pairs from five mammoths, 14 Asian and eight African elephants. A high degree of polymorphism is detected within species. With a dugong sequence used as the outgroup, parsimony and maximum-likelihood analyses support a mammoth African elephant clade. As the dugong is a very distant outgroup, we employ likelihood analysis to root the tree with a molecular clock, and use bootstrap and Bayesian analyses to quantify the relative support for different topologies. The analyses support the mammoth African elephant relationship, although other trees cannot be rejected. Ancestral polymorphisms may have resulted in gene trees differing from the species phylogeny Examination of morphological data, especially from primitive fossil members, indicates that some supposed synapomorphies between the mammoth and Asian elephant are variable, others convergent or autapomorphous. A mammoth African elephant relationship is not excluded. Our results highlight the need, in both morphological and molecular phylogenetics, for multiple markers and close attention to within-taxon variation and outgroup selection.     

Survey of the reproductive cyclicity status of Asian and African elephants in North America

The Asian and African elephant populations in North America are not self‐sustaining, and reproductive rates remain low. One problem identified from routine progestagen analyses is that some elephant females do not exhibit normal ovarian cycles. To better understand the extent of this problem, the Elephant TAG/SSP conducted a survey to determine the reproductive status of the captive population based on hormone and ultrasound evaluations. The survey response rates for facilities with Asian and African elephants were 81% and 71%, respectively, for the studbook populations, and nearly 100% for the SSP facilities. Of the elephants surveyed, 49% of Asian and 62% of African elephant females were being monitored for ovarian cyclicity via serum or urinary progestagen analyses on a weekly basis. Of these, 14% of Asian and 29% of African elephants either were not cycling at all or exhibited irregular cycles. For both species, ovarian inactivity was more prevalent in the older age categories (>30 years); however, acyclicity was found in all age groups of African elephants. Fewer elephant females (～30%) had been examined by transrectal ultrasound to assess reproductive‐tract integrity, and corresponding hormonal data were available for about three‐quarters of these females. Within this subset, most (～75%) cycling females had normal reproductive‐tract morphologies, whereas at least 70% of noncycling females exhibited some type of ovarian or uterine pathology. In summary, the survey results suggest that ovarian inactivity is a significant reproductive problem for elephants held in zoos, especially African elephants. To increase the fecundity of captive elephants, females should be bred at a young age, before reproductive pathologies occur. However, a significant number of older Asian elephants are still not being reproductively monitored. More significantly, many prime reproductive‐age (10–30 years) African females are not being monitored. This lack of information makes it difficult to determine what factors affect the reproductive health of elephants, and to develop mitigating treatments to reinitiate reproductive cyclicity. Zoo Biol 23:309–321, 2004. © 2004 Wiley‐Liss, Inc.     

象科动物对当地森林生态系统的影响

现存的象科动物(Elephantidae)分为非洲草原象(Loxodonta africana)、非洲森林象(Loxodonta cyclotis)和亚洲象(Elephas maximus)3 种,作为森林生态系统的关键物种,它们对当地森林生态系统的影响非常复杂,在一定环境条件下,既可能是积极的作用,也可能是消极的作用。积极的作用包括:帮助植物传播种子;促进种子萌发;创造断层,维持群落多样性;为其他动物增加食物资源;为其他动物创造栖息地。消极的作用包括:使一些物种的种群数量减小;使森林变成灌木丛和草原等。而由于活动受限导致的种群密度过高是象科动物对森林生态系统产生消极作用的主要原因。当前象科动物的3 个物种均面临种群数量锐减和生存空间不断缩小的危机,为此迫切需要针对其对生物多样性和生态平衡的影响开展深入和全面的研究,并且应根据实际情况因地制宜地制定管理措施。     

The historical development of zoo elephant survivorship

In the discussion about zoo elephant husbandry, the report of Clubb et al. (2008, Science 322: 1649) that zoo elephants had a “compromised survivorship” compared to certain non-zoo populations is a grave argument, and was possibly one of the triggers of a large variety of investigations into zoo elephant welfare, and changes in zoo elephant management. A side observation of that report was that whereas survivorship in African elephants (Loxodonta africana) improved since 1960, this was not the case in Asian elephants (Elephas maximus). We used historical data (based on the Species360 database) to revisit this aspect, including recent developments since 2008. Assessing the North American and European populations from 1910 until today, there were significant improvements of adult (≥10 years) survivorship in both species. For the period from 1960 until today, survivorship improvement was significant for African elephants and close to a significant improvement in Asian elephants; Asian elephants generally had a higher survivorship than Africans. Juvenile (<10 years) survivorship did not change significantly since 1960 and was higher in African elephants, most likely due to the effect of elephant herpes virus on Asian elephants. Current zoo elephant survivorship is higher than some, and lower than some other non-zoo populations. We discuss that in our view, the shape of the survivorship curve, and its change over time, are more relevant than comparisons with specific populations. Zoo elephant survivorship should be monitored continuously, and the expectation of a continuous trend towards improvement should be met.     

Bee Threat Elicits Alarm Call in African Elephants

Unlike the smaller and more vulnerable mammals, African elephants have relatively few predators that threaten their survival. The sound of disturbed African honeybees Apis meliffera scutellata causes African elephants Loxodonta africana to retreat and produce warning vocalizations that lead other elephants to join the flight. In our first experiment, audio playbacks of bee sounds induced elephants to retreat and elicited more head-shaking and dusting, reactive behaviors that may prevent bee stings, compared to white noise control playbacks. Most importantly, elephants produced distinctive “rumble” vocalizations in response to bee sounds. These rumbles exhibited an upward shift in the second formant location, which implies active vocal tract modulation, compared to rumbles made in response to white noise playbacks. In a second experiment, audio playbacks of these rumbles produced in response to bees elicited increased headshaking, and further and faster retreat behavior in other elephants, compared to control rumble playbacks with lower second formant frequencies. These responses to the bee rumble stimuli occurred in the absence of any bees or bee sounds. This suggests that these elephant rumbles may function as referential signals, in which a formant frequency shift alerts nearby elephants about an external threat, in this case, the threat of bees.     

Personality Assessment and Its Association With Genetic Factors in Captive Asian and African Elephants

Elephants live in a complex society based on matrilineal groups. Management of captive elephants is difficult, partly because each elephant has a unique personality. For a better understanding of elephant well being in captivity, it would be helpful to systematically evaluate elephants' personalities and their underlying biological basis. We sent elephant' personality questionnaires to keepers of 75 elephants. We also used 196 elephant DNA samples to search for genetic polymorphisms in genes expressed in the brain that have been suggested to be related to personality traits. Three genes, androgen receptor (AR), fragile X related mental retardation protein interacting protein (NUFIP2), and acheate‐scute homologs 1 (ASH1) contained polymorphic regions. We examined the association of personality with intraspecific genetic variation in 17 Asian and 28 African elephants. The results suggest that the ASH1 genotype was associated with neuroticism in Asian elephants. Subjects with short alleles had lower scores of neuroticism than those with long alleles. This is the first report of an association between a genetic polymorphism and personality in elephants. Zoo Biol. 32:70‐78, 2013. © 2012 Wiley Periodicals, Inc.     

Genomic inferences from Afrotheria and the evolution of elephants

Recent genetic studies have established that African forest and savanna elephants are distinct species with dissociated cytonuclear genomic patterns, and have identified Asian elephants from Borneo and Sumatra as conservation priorities. Representative of Afrotheria, a superordinal clade encompassing six eutherian orders, the African savanna elephant was among the first mammals chosen for whole-genome sequencing to provide a comparative understanding of the human genome. Elephants have large and complex brains and display advanced levels of social structure, communication, learning and intelligence. The elephant genome sequence might prove useful for comparative genomic studies of these advanced traits, which have appeared independently in only three mammalian orders: primates, cetaceans and proboscideans.     

Reconciling apparent conflicts between mitochondrial and nuclear phylogenies in African elephants

Conservation strategies for African elephants would be advanced by resolution of conflicting claims that they comprise one, two, three or four taxonomic groups, and by development of genetic markers that establish more incisively the provenance of confiscated ivory. We addressed these related issues by genotyping 555 elephants from across Africa with microsatellite markers, developing a method to identify those loci most effective at geographic assignment of elephants (or their ivory), and conducting novel analyses of continent-wide datasets of mitochondrial DNA. Results showed that nuclear genetic diversity was partitioned into two clusters, corresponding to African forest elephants (99.5% Cluster-1) and African savanna elephants (99.4% Cluster-2). Hybrid individuals were rare. In a comparison of basal forest "F" and savanna "S" mtDNA clade distributions to nuclear DNA partitions, forest elephant nuclear genotypes occurred only in populations in which S clade mtDNA was absent, suggesting that nuclear partitioning corresponds to the presence or absence of S clade mtDNA. We reanalyzed African elephant mtDNA sequences from 81 locales spanning the continent and discovered that S clade mtDNA was completely absent among elephants at all 30 sampled tropical forest locales. The distribution of savanna nuclear DNA and S clade mtDNA corresponded closely to range boundaries traditionally ascribed to the savanna elephant species based on habitat and morphology. Further, a reanalysis of nuclear genetic assignment results suggested that West African elephants do not comprise a distinct third species. Finally, we show that some DNA markers will be more useful than others for determining the geographic origins of illegal ivory. These findings resolve the apparent incongruence between mtDNA and nuclear genetic patterns that has confounded the taxonomy of African elephants, affirm the limitations of using mtDNA patterns to infer elephant systematics or population structure, and strongly support the existence of two elephant species in Africa.