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Concept: Elephantidae

158

The capacity to recognise oneself as separate from other individuals and objects is difficult to investigate in non-human animals. The hallmark empirical assessment, the mirror self-recognition test, focuses on an animal’s ability to recognise itself in a mirror and success has thus far been demonstrated in only a small number of species with a keen interest in their own visual reflection. Adapting a recent study done with children, we designed a new body-awareness paradigm for testing an animal’s understanding of its place in its environment. In this task, Asian elephants (Elephas maximus) were required to step onto a mat and pick up a stick attached to it by rope, and then pass the stick forward to an experimenter. In order to do the latter, the elephants had to see their body as an obstacle to success and first remove their weight from the mat before attempting to transfer the stick. The elephants got off the mat in the test significantly more often than in controls, where getting off the mat was unnecessary. This task helps level the playing field for non-visual species tested on cognition tasks and may help better define the continuum on which body- and self-awareness lie.

Concepts: Mammal, Elephant, Asian Elephant, Elephas, Elephantidae, Sri Lankan Elephant, Elephants, Mirror test

95

Woolly mammoths and living elephants are characterized by major phenotypic differences that have allowed them to live in very different environments. To identify the genetic changes that underlie the suite of woolly mammoth adaptations to extreme cold, we sequenced the nuclear genome from three Asian elephants and two woolly mammoths, and we identified and functionally annotated genetic changes unique to woolly mammoths. We found that genes with mammoth-specific amino acid changes are enriched in functions related to circadian biology, skin and hair development and physiology, lipid metabolism, adipose development and physiology, and temperature sensation. Finally, we resurrected and functionally tested the mammoth and ancestral elephant TRPV3 gene, which encodes a temperature-sensitive transient receptor potential (thermoTRP) channel involved in thermal sensation and hair growth, and we show that a single mammoth-specific amino acid substitution in an otherwise highly conserved region of the TRPV3 channel strongly affects its temperature sensitivity.

Concepts: DNA, Protein, Gene, Genetics, Genome, Elephantidae, Mammoth, Woolly mammoth

75

Large mammalian terrestrial herbivores, such as elephants, have dramatic effects on the ecosystems they inhabit and at high population densities their environmental impacts can be devastating. Pleistocene terrestrial ecosystems included a much greater diversity of megaherbivores (e.g., mammoths, mastodons, giant ground sloths) and thus a greater potential for widespread habitat degradation if population sizes were not limited. Nevertheless, based on modern observations, it is generally believed that populations of megaherbivores (>800 kg) are largely immune to the effects of predation and this perception has been extended into the Pleistocene. However, as shown here, the species richness of big carnivores was greater in the Pleistocene and many of them were significantly larger than their modern counterparts. Fossil evidence suggests that interspecific competition among carnivores was relatively intense and reveals that some individuals specialized in consuming megaherbivores. To estimate the potential impact of Pleistocene large carnivores, we use both historic and modern data on predator-prey body mass relationships to predict size ranges of their typical and maximum prey when hunting as individuals and in groups. These prey size ranges are then compared with estimates of juvenile and subadult proboscidean body sizes derived from extant elephant growth data. Young proboscideans at their most vulnerable age fall within the predicted prey size ranges of many of the Pleistocene carnivores. Predation on juveniles can have a greater impact on megaherbivores because of their long interbirth intervals, and consequently, we argue that Pleistocene carnivores had the capacity to, and likely did, limit megaherbivore population sizes.

Concepts: Predation, Mammal, Population density, Lion, Hunting, Carnivore, Elephantidae, Mammoth

71

Concerns about animal welfare increasingly shape people’s views about the acceptability of keeping animals for food production, biomedical research, and in zoos. The field of animal welfare science has developed over the past 50 years as a method of investigating these concerns via research that assesses how living in human-controlled environments influences the behavior, health and affective states of animals. Initially, animal welfare research focused on animals in agricultural settings, but the field has expanded to zoos because good animal welfare is essential to zoos' mission of promoting connections between animals and visitors and raising awareness of conservation issues. A particular challenge for zoos is ensuring good animal welfare for long-lived, highly social species like elephants. Our main goal in conducting an epidemiological study of African (Loxodonta africana) and Asian (Elephas maximus) elephant welfare in 68 accredited North American zoos was to understand the prevalence of welfare indicators in the population and determine the aspects of an elephant’s zoo environment, social life and management that are most important to prevent and reduce a variety of welfare problems. In this overview, we provide a summary of the findings of the nine papers in the collection titled: Epidemiological Investigations of North American Zoo Elephant Welfare with a focus on the life history, social, housing, and management factors found to be associated with particular aspects of elephant welfare, including the performance of abnormal behavior, foot and joint problems, recumbence, walking rates, and reproductive health issues. Social and management factors were found to be important for multiple indicators of welfare, while exhibit space was found to be less influential than expected. This body of work results from the largest prospective zoo-based animal welfare study conducted to date and sets in motion the process of using science-based welfare benchmarks to optimize care of zoo elephants.

Concepts: Elephant, Asian Elephant, Elephas, Elephantidae, Elephants, Animal welfare, African Bush Elephant, Zoo

38

For more than three decades, foot and musculoskeletal conditions have been documented among both Asian [Elephas maximus] and African [Loxodonta africana] elephants in zoos. Although environmental factors have been hypothesized to play a contributing role in the development of foot and musculoskeletal pathology, there is a paucity of evidence-based research assessing risk. We investigated the associations between foot and musculoskeletal health conditions with demographic characteristics, space, flooring, exercise, enrichment, and body condition for elephants housed in North American zoos during 2012. Clinical examinations and medical records were used to assess health indicators and provide scores to quantitate conditions. Using multivariable regression models, associations were found between foot health and age [P value = 0.076; Odds Ratio = 1.018], time spent on hard substrates [P value = 0.022; Odds Ratio = 1.014], space experienced during the night [P value = 0.041; Odds Ratio = 1.008], and percent of time spent in indoor/outdoor exhibits during the day [P value < 0.001; Odds Ratio = 1.003]. Similarly, the main risk factors for musculoskeletal disorders included time on hard substrate [P value = 0.002; Odds Ratio = 1.050] and space experienced in indoor/outdoor exhibits [P value = 0.039; Odds Ratio = 1.037]. These results suggest that facility and management changes that decrease time spent on hard substrates will improve elephant welfare through better foot and musculoskeletal health.

Concepts: Elephant, Asian Elephant, Elephas, Elephantidae, Elephants, African elephant, African Bush Elephant, EDGE Species

33

Elephantids are the world’s most iconic megafaunal family, yet there is no comprehensive genomic assessment of their relationships. We report a total of 14 genomes, including 2 from the American mastodon, which is an extinct elephantid relative, and 12 spanning all three extant and three extinct elephantid species including an ∼120,000-y-old straight-tusked elephant, a Columbian mammoth, and woolly mammoths. Earlier genetic studies modeled elephantid evolution via simple bifurcating trees, but here we show that interspecies hybridization has been a recurrent feature of elephantid evolution. We found that the genetic makeup of the straight-tusked elephant, previously placed as a sister group to African forest elephants based on lower coverage data, in fact comprises three major components. Most of the straight-tusked elephant’s ancestry derives from a lineage related to the ancestor of African elephants while its remaining ancestry consists of a large contribution from a lineage related to forest elephants and another related to mammoths. Columbian and woolly mammoths also showed evidence of interbreeding, likely following a latitudinal cline across North America. While hybridization events have shaped elephantid history in profound ways, isolation also appears to have played an important role. Our data reveal nearly complete isolation between the ancestors of the African forest and savanna elephants for ∼500,000 y, providing compelling justification for the conservation of forest and savanna elephants as separate species.

Concepts: Gene, Elephant, Elephantidae, African Bush Elephant, Mammoth, Prehistoric elephants, Pleistocene mammals, Mastodon

31

Tuberculosis is an important health concern for Asian elephant (Elephas maximus) populations worldwide, however, mechanisms underlying susceptibility to Mycobacterium tuberculosis are unknown. Proliferative responses assessed via brominated uridine incorporation and cytokine expression measured by real-time RT-PCR were evaluated in peripheral blood mononuclear cell (PBMC) cultures from 8 tuberculosis negative and 8 positive Asian elephants. Cultures were stimulated with Mycobacterium bovis purified protein derivative (PPD-B), M. tuberculosis culture filtrate protein (CFP)-10, and Mycobacterium avium PPD (PPD-A). Following stimulation with PPD-B, proliferation was higher (α = 0.005) in positive samples; no significant differences were detected following CFP-10 or PPD-A stimulation. Tumor necrosis factor (TNF)-α, interleukin (IL)-12, and interferon (IFN)-γ expression was greater in samples from positive elephants following stimulation with PPD-B (α = 0.025) and CFP-10 (α = 0.025 TNF-α and IL-12; α = 0.005 IFN-γ). Stimulation with PPD-A also produced enhanced IL-12 expression in positive samples (α = 0.025). Findings suggested that differences in immune cell function exist between tuberculosis positive and negative elephants. Proliferative responses and expression of TNF-α, IL-12, and IFN-γ in response to stimulation with PPD-B and CFP-10 differ between tuberculosis positive and negative elephants, suggesting these parameters may be important to tuberculosis immunopathogenesis in this species.

Concepts: Tuberculosis, Mycobacterium, Elephant, Asian Elephant, Elephas, Elephantidae, Sri Lankan Elephant, War elephant

25

Maintaining adequate welfare in captive elephants is challenging. Few studies have investigated overnight rest behavior in zoo elephants, yet time spent resting has been identified as a welfare indicator in some species. We investigated resting behavior in Asian elephants (Elephas maximus) in UK zoos, with the aim of identifying patterns or preferences in lying rest. Details of standing (SR) and lying (LR) rest behavior were identified by observing video footage of inside enclosures collected for 14 elephants (2 male, 12 female) housed at three UK zoos (Zoo A: 18 nights; Zoo B: 27 nights; Zoo C: 46 nights) from 16:00 to 08:30 (approximately). Elephants engaged in a mean of 58-337 min rest per night. Time of night affected mean duration of LR bouts (P < 0.001); longest bouts were observed between 22:01 and 06:00. Elephants showed a substrate preference when lying to rest; LR was not observed on concrete or tiled flooring. Where sand was available (to 11/14 elephants), all elephants engaged in LR on sand flooring. Only two elephants engaged in LR on rubber flooring (available to 7/14 elephants). Mean duration of rest bouts was greater when a conspecific was within two body lengths than when conspecifics were not (P < 0.01). Our study indicated that elephants show substrate preferences when choosing an area for rest and engage in more rest when conspecifics are in close proximity. The results of this study could be used as a basis for future studies investigating the link between rest and welfare in captive elephants. Zoo Biol. XX:XX-XX, 2015. © 2015 Wiley Periodicals, Inc.

Concepts: Elephant, Asian Elephant, Elephas, Elephantidae, Sri Lankan Elephant, Elephants, War elephant, Borneo Elephant

22

The management of African (Loxodonta africana) and Asian (Elephas maximus) elephants in zoos involves a range of practices including feeding, exercise, training, and environmental enrichment. These practices are necessary to meet the elephants' nutritional, healthcare, and husbandry needs. However, these practices are not standardized, resulting in likely variation among zoos as well as differences in the way they are applied to individual elephants within a zoo. To characterize elephant management in North America, we collected survey data from zoos accredited by the Association of Zoos and Aquariums, developed 26 variables, generated population level descriptive statistics, and analyzed them to identify differences attributable to sex and species. Sixty-seven zoos submitted surveys describing the management of 224 elephants and the training experiences of 227 elephants. Asian elephants spent more time managed (defined as interacting directly with staff) than Africans (mean time managed: Asians = 56.9%; Africans = 48.6%; p<0.001), and managed time increased by 20.2% for every year of age for both species. Enrichment, feeding, and exercise programs were evaluated using diversity indices, with mean scores across zoos in the midrange for these measures. There were an average of 7.2 feedings every 24-hour period, with only 1.2 occurring during the nighttime. Feeding schedules were predictable at 47.5% of zoos. We also calculated the relative use of rewarding and aversive techniques employed during training interactions. The population median was seven on a scale from one (representing only aversive stimuli) to nine (representing only rewarding stimuli). The results of our study provide essential information for understanding management variation that could be relevant to welfare. Furthermore, the variables we created have been used in subsequent elephant welfare analyses.

Concepts: North America, Elephant, Asian Elephant, Elephas, Elephantidae, Elephants, War elephant, African elephant

21

Recent research suggests that domesticated species - due to artificial selection by humans for specific, preferred behavioral traits - are better than wild animals at responding to visual cues given by humans about the location of hidden food. \Although this seems to be supported by studies on a range of domesticated (including dogs, goats and horses) and wild (including wolves and chimpanzees) animals, there is also evidence that exposure to humans positively influences the ability of both wild and domesticated animals to follow these same cues. Here, we test the performance of Asian elephants (Elephas maximus) on an object choice task that provides them with visual-only cues given by humans about the location of hidden food. Captive elephants are interesting candidates for investigating how both domestication and human exposure may impact cue-following as they represent a non-domesticated species with almost constant human interaction. As a group, the elephants (n = 7) in our study were unable to follow pointing, body orientation or a combination of both as honest signals of food location. They were, however, able to follow vocal commands with which they were already familiar in a novel context, suggesting the elephants are able to follow cues if they are sufficiently salient. Although the elephants' inability to follow the visual cues provides partial support for the domestication hypothesis, an alternative explanation is that elephants may rely more heavily on other sensory modalities, specifically olfaction and audition. Further research will be needed to rule out this alternative explanation.

Concepts: Genetic pollution, Domestication, Elephant, Asian Elephant, Elephas, Elephantidae, War elephant, Wildness