Testosterone histories from tusks reveal woolly mammoth musth episodes.

Hormones in biological media reveal endocrine activity related to development, reproduction, disease and stress on different timescales1. Serum provides immediate circulating concentrations2, whereas various tissues record steroid hormones accumulated over time3,4. Hormones have been studied in keratin, bones and teeth in modern5-8 and ancient contexts9-12; however, the biological significance of such records is subject to ongoing debate10,13-16, and the utility of tooth-associated hormones has not previously been demonstrated. Here we use liquid chromatography with tandem mass spectrometry paired with fine-scale serial sampling to measure steroid hormone concentrations in modern and fossil tusk dentin. An adult male African elephant (Loxodonta africana) tusk shows periodic increases in testosterone that reveal episodes of musth17-19, an annually recurring period of behavioural and physiological changes that enhance mating success20-23. Parallel assessments of a male woolly mammoth (Mammuthus primigenius) tusk show that mammoths also experienced musth. These results set the stage for wide-ranging studies using steroids preserved in dentin to investigate development, reproduction and stress in modern and extinct mammals. Because dentin grows by apposition, resists degradation, and often contains growth lines, teeth have advantages over other tissues that are used as records of endocrine data. Given the low mass of dentin powder required for analytical precision, we anticipate dentin-hormone studies to extend to smaller animals. Thus, in addition to broad applications in zoology and palaeontology, tooth hormone records could support medical, forensic, veterinary and archaeological studies.

Shape variation in the limb long bones of modern elephants reveals adaptations to body mass and habitat.

During evolution, several vertebrate lineages have shown trends towards an increase in mass. Such a trend is associated with physiological and musculoskeletal changes necessary to carry and move an increasingly heavy body. Due to their prominent role in the support and movement of the body, limb long bones are highly affected by these shifts in body mass. Elephants are the heaviest living terrestrial mammals, displaying unique features allowing them to withstand their massive weight, such as the columnarity of their limbs, and as such are crucial to understand the evolution towards high body mass in land mammals. In this study, we investigate the shape variation of the six limb long bones among the modern elephants, Elephas maximus and Loxodonta africana, to understand the effect of body mass and habitat on the external anatomy of the bones. To do so, we use three-dimensional geometric morphometrics (GMMs) and qualitative comparisons to describe the shape variation, at both the intraspecific and interspecific levels. Our results reveal that the two species share similar negative ontogenetic allometric patterns (i.e. becoming stouter with increased length) in their humerus and femur, but not in the other bones: the proximal epiphyses of the stylopod bones develop considerably during growth, while the distal epiphyses, which are involved in load distribution in the elbow and knee joints, are already massive in juveniles. We attribute this pattern to a weight-bearing adaptation already present in young specimens. Among adults of the same species, bone robustness increases with body mass, so that heavier specimens display stouter bones allowing for a better mechanical load distribution. While this robustness variation is significant for the humerus only, all the other bones appear to follow the same pattern. This is particularly visible in the ulna and tibia, but less so in the femur, which suggests that the forelimb and hindlimb adapted differently to high body mass support. Robustness analyses, while significant for the humerus only, suggest more robust long bones in Asian elephants than in African savanna elephants. More specifically, GMMs and qualitative comparisons indicate that three bones are clearly distinct when comparing the two species: in E. maximus the humerus, the ulna and the tibia display enlarged areas of muscular insertions for muscles involved in joint and limb stabilization, as well as in limb rotation. These results suggest a higher limb compliance in Asian elephants, associated with a higher dexterity, which could be linked to their habitat and foraging habits.

Skin wrinkles and folds enable asymmetric stretch in the elephant trunk.

The elephant's trunk is multifunctional: It must be flexible to wrap around vegetation, but tough to knock down trees and resist attack. How can one appendage satisfy both constraints? In this combined experimental and theoretical study, we challenged African elephants to reach far-away objects with only horizontal extensions of their trunk. Surprisingly, the trunk does not extend uniformly, but instead exhibits a dorsal "joint" that stretches 15% more than the corresponding ventral section. Using material testing with the skin of a deceased elephant, we show that the asymmetry is due in part to patterns of the skin. The dorsal skin is folded and 15% more pliable than the wrinkled ventral skin. Skin folds protect the dorsal section and stretch to facilitate downward wrapping, the most common gripping style when picking up items. The elephant's skin is also sufficiently stiff to influence its mechanics: At the joint, the skin requires 13 times more energy to stretch than the corresponding length of muscle. The use of wrinkles and folds to modulate stiffness may provide a valuable concept for both biology and soft robotics.

CT anatomy of cervical vertebrae of Asian elephant (Elephas maximus).

BACKGROUND: Elephants are currently the largest mammals on earth. A comprehensive examination of the anatomy of this animal to diagnose various disorders is required. In addition, due to the heavy head of these animals, adaptations have been made in the anatomical structure of the neck that is worth studying. OBJECTIVE: This study aimed to investigate a standard morphologic and morphometric description of the elephant cervical spine. Another aim of this study was to compare the changes in the cervical skeleton of elephants with horses and cattle. METHODS: For this study, the cervical vertebrae of the Asian elephant, cattle and horse were examined. CT Images were obtained using Somatom Spirit II CT Machine. Statistical analysis was done by SPSS 24 software. RESULTS: Two dorsal tubercles and a groove between them were observed on the dorsal arch of the atlas vertebra of the Asian elephant. In elephant samples, the variation of vertebral body height, spinous process height, transverse process width, vertebral body length and vertebral foramen volume indices were statistically significant. The volume of the vertebral foramen in the elephant decreases in the second vertebra compared to the first vertebra, decreases in the third vertebra, decreases in the fourth, increases in the fifth, decreases in the sixth and increases in the seventh. CONCLUSIONS: In this study, the structure of the cervical vertebrae of the Asian elephant was examined, and certain features were observed. One of the main features was the reduction of the length of the vertebrae, which leads to the decrease of the ratio of neck length to the size of the body. This condition can be due to the high weight of the head in the elephant. To maintain this weight, it is necessary to reduce the length of the neck and confer less mobility.

The relationship between distal trunk morphology and object grasping in the African savannah elephant (Loxodonta africana).

Background: During reach-to-grasp movements, the human hand is preshaped depending on the properties of the object. Preshaping may result from learning, morphology, or motor control variability and can confer a selective advantage on that individual or species. This preshaping ability is known in several mammals (i.e., primates, carnivores and rodents). However, apart from the tongue preshaping of lizards and chameleons, little is known about preshaping of other grasping appendages. In particular, the elephant trunk, a muscular hydrostat, has impressive grasping skills and thus is commonly called a hand. Data on elephant trunk grasping strategies are scarce, and nothing is known about whether elephants preshape their trunk tip according to the properties of their food. Methods: To determine the influence of food sizes and shapes on the form of the trunk tip, we investigated the morphology of the distal part of the trunk during grasping movements. The influence of food item form on trunk tip shape was quantified in six female African savannah elephants (Loxodonta africana). Three food item types were presented to the elephants (elongated, flat, and cubic), as well as three different sizes of cubic items. A total of 107 ± 10 grips per individual were video recorded, and the related trunk tip shapes were recorded with a 2D geometric morphometric approach. Results: Half of the individuals adjusted the shape of the distal part of their trunk according to the object type. Of the three elephants that did not preshape their trunk tip, one was blind and another was subadult. Discussion and perspectives: We found that elephants preshaped their trunk tip, similar to the preshaping of other species' hands or paws during reach-to-grasp movements. This preshaping may be influenced by visual feedback and individual learning. To confirm these results, this study could be replicated with a larger sample of elephants.

Ivory poaching and the rapid evolution of tusklessness in African elephants.

Understanding the evolutionary consequences of wildlife exploitation is increasingly important as harvesting becomes more efficient. We examined the impacts of ivory poaching during the Mozambican Civil War (1977 to 1992) on the evolution of African savanna elephants (Loxodonta africana) in Gorongosa National Park. Poaching resulted in strong selection that favored tusklessness amid a rapid population decline. Survey data revealed tusk-inheritance patterns consistent with an X chromosome­linked dominant, male-lethal trait. Whole-genome scans implicated two candidate genes with known roles in mammalian tooth development (AMELX and MEP1a), including the formation of enamel, dentin, cementum, and the periodontium. One of these loci (AMELX) is associated with an X-linked dominant, male-lethal syndrome in humans that diminishes the growth of maxillary lateral incisors (homologous to elephant tusks). This study provides evidence for rapid, poaching-mediated selection for the loss of a prominent anatomical trait in a keystone species.

First tracks of newborn straight-tusked elephants (Palaeoloxodon antiquus).

Tracks and trackways of newborns, calves and juveniles attributed to straight-tusked elephants were found in the MIS 5 site (Upper Pleistocene) known as the Matalascañas Trampled Surface (MTS) at Huelva, SW Spain. Evidence of a snapshot of social behaviour, especially parental care, can be determined from the concentration of elephant tracks and trackways, and especially from apparently contemporaneous converging trackways, of small juvenile and larger, presumably young adult female tracks. The size frequency of the tracks enabled us to infer body mass and age distribution of the animals that crossed the MTS. Comparisons of the MTS demographic frequency with the morphology of the fore- and hind limbs of extant and fossil proboscideans shed light into the reproductive ecology of the straight-tusked elephant, Palaeloxodon antiquus. The interdune pond habitat appeared to have been an important water and food resource for matriarchal herds of straight-tusked elephants and likely functioned as a reproductive habitat, with only the rare presence of adult and older males in the MTS. The preservation of this track record in across a paleosol surface, although heavily trampled by different animals, including Neanderthals, over a short time frame, permitted an exceptional view into short-term intraspecific trophic interactions occurring in the Last Interglacial coastal habitat. Therefore, it is hypothesized that Neanderthals visited MTS for hunting or scavenging on weakened or dead elephants, and more likely calves.

Elephant bones for the Middle Pleistocene toolmaker.

The use of bone as raw material for implements is documented since the Early Pleistocene. Throughout the Early and Middle Pleistocene bone tool shaping was done by percussion flaking, the same technique used for knapping stone artifacts, although bone shaping was rare compared to stone tool flaking. Until recently the generally accepted idea was that early bone technology was essentially immediate and expedient, based on single-stage operations, using available bone fragments of large to medium size animals. Only Upper Paleolithic bone tools would involve several stages of manufacture with clear evidence of primary flaking or breaking of bone to produce the kind of fragments required for different kinds of tools. Our technological and taphonomic analysis of the bone assemblage of Castel di Guido, a Middle Pleistocene site in Italy, now dated by 40Ar/39Ar to about 400 ka, shows that this general idea is inexact. In spite of the fact that the number of bone bifaces at the site had been largely overestimated in previous publications, the number of verified, human-made bone tools is 98. This is the highest number of flaked bone tools made by pre-modern hominids published so far. Moreover the Castel di Guido bone assemblage is characterized by systematic production of standardized blanks (elephant diaphysis fragments) and clear diversity of tool types. Bone smoothers and intermediate pieces prove that some features of Aurignacian technology have roots that go beyond the late Mousterian, back to the Middle Pleistocene. Clearly the Castel di Guido hominids had done the first step in the process of increasing complexity of bone technology. We discuss the reasons why this innovation was not developed. The analysis of the lithic industry is done for comparison with the bone industry.

Weigh and see-Body mass recordings versus body condition scoring in European zoo elephants (Loxodonta africana and Elephas maximus).

Regular body mass (BM) monitoring plays a key role in preventative health care of zoo animals. In some species, including African (Loxodonta africana) and Asian elephants (Elephas maximus), the process of weighing can be challenging, and alternative methods such as visual body condition scoring (BCS) have been developed. We investigated the temporal development of both parameters regarding correlation patterns between them, and their suitability as monitoring measures in dependence of an elephant's life stage. While BM is more suitable in calves and juveniles under the age of 8 years, both BM and BCS are considered equally reliable in adult elephants. In elephants over the age of 40 years, BCS might be more suitable for assessing the physical status. Independent of species and sex, juvenile zoo elephants grow in BM nearly linearly with age, and reach a higher BM at an earlier age compared with conspecifics of free-ranging and semi-captive populations in the countries of origin. The BCS typically remains constant during this life stage, seemingly unaffected by growth. In adult animals, breeding females have a lower BM and BCS than nonbreeders, and BM and BCS typically indicate fluctuations in the same direction. In geriatric elephants (>40 years) a drop in BCS occurs commonly, while BM may even increase in this life stage. We recommend regular body mass recording in zoo elephants to enhance our knowledge of body mass development and allow the formulation of objective practical recommendations. BCS presents a valuable and simple tool for complementary monitoring of an elephant's condition, especially in adult and geriatric individuals.

EVALUATION OF THE BONE MINERAL DENSITY OF ASIAN ELEPHANTS (ELEPHAS MAXIMUS) VIA DUAL-ENERGY X-RAY IMAGING OF TAILS.

Musculoskeletal problems are one of the top five causes of disease in elephants. However, recent blood chemistry analysis is the only routine protocol for bone mineral status evaluation, with no assessment method currently available for the direct measurement of elephant bone mineral density (BMD). This work applied the the dual-energy X-ray technique (DXA) technique for bone density assessment. The elephant's tail was chosen for the analysis to avoid the radiation harm. Twelve live Asian elephants (Elephas maximus) comprising eight males and four females with ages in the range of 4-77 yr were investigated. The BMD was calculated based on radiographic images acquired using the DXA technique carried out at 40 kVp 2 mAs and 50 kVp 2 mAs. Blood serum analysis of total calcium (Ca), phosphorus (Phos) and alkaline phosphatase (ALP) content was conducted in parallel with the physical examination to correlate age and BMD. Analyses produced an overall mean BMD value in the range of 0.54-1.39 g/cm2, with that of the males higher than that of the females. The BMD was found to be negatively correlated with age, Ca, and Phos, but not with ALP. In summary, the BMD analysis of an elephant's tail might be used with blood serum Ca and Phos to predict the overall bone mineral status of the animal.

Arcuate foramen: "Anatomical variation shape or adaptation legacy?"

PURPOSE: The groove of the vertebral artery on the posterior arch of the atlas (sulcus arteriae vertebralis) may become a complete or partial osseous foramen: the arcuate foramen. The presence of a complete or partial arcuate foramen is a rare anatomical variant described in a minority of patients and it seems to be associated with vertigo, vertebro-basilar insufficiency, posterior circulation strokes, and musculoskeletal pain. As the number and morphology of cervical vertebrae is highly preserved, we questioned about its significance from an evolutionary point of view. We thus investigated through an extensive literature review if the arcuate foramen is a pure anatomical variation shape or if it might represent an adaptation legacy. METHODS: We observed five atlas of an extinct species, the Late Pleistocene Mammoths (M. primigenius), and we compared them with five atlas of a closely related existent species, the African elephant (L. africana). RESULTS: All the mammoths' atlas had an arcuate foramen through which the vertebral artery passed before turning anteriorly and becoming intradural. This foramen was not present in elephants' atlas, where only a groove was observed, such as in the majority of patients. CONCLUSION: We would like to raise the hypothesis that this peculiar morphology of mammoths' atlas might have contributed, in association with other factors, to their precocious extinction and that the arcuate foramen might represent a disadvantage in the evolutionary process, with a low prevalence in humans being the result of a natural selection.

Locally-curved geometry generates bending cracks in the African elephant skin.

An intricate network of crevices adorns the skin surface of the African bush elephant, Loxodonta africana. These micrometre-wide channels enhance the effectiveness of thermal regulation (by water retention) as well as protection against parasites and intense solar radiation (by mud adherence). While the adaptive value of these structures is well established, their morphological characterisation and generative mechanism are unknown. Using microscopy, computed tomography and a custom physics-based lattice model, we show that African elephant skin channels are fractures of the animal brittle and desquamation-deficient skin outermost layer. We suggest that the progressive thickening of the hyperkeratinised stratum corneum causes its fracture due to local bending mechanical stress in the troughs of a lattice of skin millimetric elevations. The African elephant skin channels are therefore generated by thickening of a brittle material on a locally-curved substrate rather than by a canonical tensile cracking process caused by frustrated shrinkage.

A grazing Gomphotherium in Middle Miocene Central Asia, 10 million years prior to the origin of the Elephantidae.

Feeding preference of fossil herbivorous mammals, concerning the coevolution of mammalian and floral ecosystems, has become of key research interest. In this paper, phytoliths in dental calculus from two gomphotheriid proboscideans of the middle Miocene Junggar Basin, Central Asia, have been identified, suggesting that Gomphotherium connexum was a mixed feeder, while the phytoliths from G. steinheimense indicates grazing preference. This is the earliest-known proboscidean with a predominantly grazing habit. These results are further confirmed by microwear and isotope analyses. Pollen record reveals an open steppic environment with few trees, indicating an early aridity phase in the Asian interior during the Mid-Miocene Climate Optimum, which might urge a diet remodeling of G. steinheimense. Morphological and cladistic analyses show that G. steinheimense comprises the sister taxon of tetralophodont gomphotheres, which were believed to be the general ancestral stock of derived "true elephantids"; whereas G. connexum represents a more conservative lineage in both feeding behavior and tooth morphology, which subsequently became completely extinct. Therefore, grazing by G. steinheimense may have acted as a behavior preadaptive for aridity, and allowing its lineage evolving new morphological features for surviving later in time. This study displays an interesting example of behavioral adaptation prior to morphological modification.

Muscles and fascial elements of the antebrachium and manus of the African elephant (Loxodonta africana, Blumenbach 1797): starring comparative and functional considerations.

The structure of the limbs of elephants is unusual among mammals. In African elephants (Loxodonta africana, Blumenbach 1797), the front limbs serve to support the greatest part of the body mass of the largest land animal. In this study, we present new and detailed anatomical data regarding muscular and specific fascial structures of the lower front limb which were examined by means of standard anatomical and histological techniques. The muscles and tendons of the forearm (antebrachium) and hand (manus) are tightly surrounded by thick, highly elastic fascial layers which fuse with the lacertus (lac.) fibrosus and the so-called ligamentum (lig.) humeroulnare. A well-developed musculus (m.) brachioradialis occupies the proximolateral aspect of the forearm and its tendon inserts together with the lac. fibrosus on the os carpi intermedium. The lac. fibrosus, the lig. humeroulnare and the m. flexor carpi radialis reveal a large proportion of elastic fibres. These three structures may play an important role in storing strain energy thus promoting energy-saving locomotion. On the palmar aspect of the carpus, metacarpus and digits, short flexor, abductor, adductor, lumbricales and interossei muscles are present, whereas supinator muscles are absent in all specimens. The short muscles of the hand together with specific dorsal tendons enable precise movements of specific toes.

Brain Changes during Phyletic Dwarfing in Elephants and Hippos.

Of all known insular mammals, hippos and elephants present the extremes of body size decrease, reducing to 4 and a mere 2% of their ancestral mainland size, respectively. Despite the numerous studies on these taxa, what happens to their relative brain size during phyletic dwarfing is not well known, and results are sometimes conflicting. For example, relative brain size increase has been noted in the Sicilian dwarf elephant, Palaeoloxodon falconeri, whereas relative brain size decrease has been postulated for Malagasy dwarf hippos. Here, I perform an analysis of brain, skull, and body size of 3 insular elephants (Palaeoloxodon "mnaidriensis," P. tiliensis, and P. falconeri) and 3 insular hippos (Hippopotamus madagascariensis, H. lemerlei, and H. minor) to address this issue and to test whether relative brain size in phyletic dwarf species can be predicted. The results presented here show that the encephalization of all insular elephants and hippos is higher than that of their continental relatives. P. falconeri in particular has an enormous encephalization increase, which has so far not been reported in any other insular mammal. Insular brain size cannot be reliably predicted using either static allometric or ontogenetic scaling models. The results of this study indicate that insular dwarf species follow brain-body allometric relationships different from the expected patterns seen for their mainland relatives.

Nuclear organization of the African elephant (Loxodonta africana) amygdaloid complex: an unusual mammalian amygdala.

Here we describe the nuclear organization of the African elephant amygdaloid complex using Nissl, myelin, and a range of immunohistochemical stains. The African elephant is thought to exhibit many affect-laden and social-empathic behaviours; however, to date the amygdaloid complex, which is the generator of emotional states of the brain is yet to be fully explored in the elephants. For the most part, the amygdaloid complex of the African elephant is similar to that observed in other mammals in terms of the presence of nuclei and their topological relationships; however, we did observe several specific differences in amygdaloid organization. The elephant amygdala has undergone rotation in both the coronal and sagittal planes, seemingly associated with the expansion of the temporal lobe. Numerous scalloped cell clusters, termed glomeruli, forming the intermediate nuclei of the basal, accessory basal and central nuclear groups, were occupied by structures immunopositive to doublecortin. The nuclei typically associated with the accessory olfactory system (posterior cortical nucleus and medial nuclear complex) were absent from the elephant amygdala. The anterior cortical nucleus is very large and appears to be comprised of two subdivisions. The lateral nuclear complex is expanded and has two novel subdivisions. The amygdalohippocampal area appears relatively enlarged. The numerous shared and derived characters make the elephant amygdaloid complex very unusual and unique amongst mammals, but the derived characters appear to relate to observed elephant affect-laden behaviours.

Learning dynamic models for open loop predictive control of soft robotic manipulators.

The soft capabilities of biological appendages like the arms of Octopus vulgaris and elephants' trunks have inspired roboticists to develop their robotic equivalents. Although there have been considerable efforts to replicate their morphology and behavior patterns, we are still lagging behind in replicating the dexterity and efficiency of these biological systems. This is mostly due to the lack of development and application of dynamic controllers on these robots which could exploit the morphological properties that a soft-bodied manipulator possesses. The complexity of these high-dimensional nonlinear systems has deterred the application of traditional model-based approaches. This paper provides a machine learning-based approach for the development of dynamic models for a soft robotic manipulator and a trajectory optimization method for predictive control of the manipulator in task space. To the best of our knowledge this is the first demonstration of a learned dynamic model and a derived task space controller for a soft robotic manipulator. The validation of the controller is carried out on an octopus-inspired soft manipulator simulation derived from a piecewise constant strain approximation and then experimentally on a pneumatically actuated soft manipulator. The results indicate that such an approach is promising for developing fast and accurate dynamic models for soft robotic manipulators while being applicable on a wide range of soft manipulators.

The Retina of Asian and African Elephants: Comparison of Newborn and Adult.

Elephants are precocial mammals that are relatively mature as newborns and mobile shortly after birth. To determine whether the retina of newborn elephants is capable of supporting the mobility of elephant calves, we compared the retinal structures of 2 newborn elephants (1 African and 1 Asian) and 2 adult animals of both species by immunohistochemical and morphometric methods. For the first time, we present here a comprehensive qualitative and quantitative characterization of the cellular composition of the newborn and the adult retinas of 2 elephant species. We found that the retina of elephants is relatively mature at birth. All retinal layers were well discernible, and various retinal cell types were detected in the newborns, including Müller glial cells (expressing glutamine synthetase and cellular retinal binding protein; CRALBP), cone photoreceptors (expressing S-opsin or M/L-opsin), protein kinase Cα-expressing bipolar cells, tyrosine hydroxylase-, choline acetyltransferase (ChAT)-, calbindin-, and calretinin-expressing amacrine cells, and calbindin-expressing horizontal cells. The retina of newborn elephants contains discrete horizontal cells which coexpress ChAT, calbindin, and calretinin. While the overall structure of the retina is very similar between newborn and adult elephants, various parameters change after birth. The postnatal thickening of the retinal ganglion cell axons and the increase in ganglion cell soma size are explained by the increase in body size after birth, and the decreases in the densities of neuronal and glial cells are explained by the postnatal expansion of the retinal surface area. The expression of glutamine synthetase and CRALBP in the Müller cells of newborn elephants suggests that the cells are already capable of supporting the activities of photoreceptors and neurons. As a peculiarity, the elephant retina contains both normally located and displaced giant ganglion cells, with single cells reaching a diameter of more than 50 µm in adults and therefore being almost in the range of giant retinal ganglion cells found in aquatic mammals. Some of these ganglion cells are displaced into the inner nuclear layer, a unique feature of terrestrial mammals. For the first time, we describe here the occurrence of many bistratified rod bipolar cells in the elephant retina. These bistratified bipolar cells may improve nocturnal contrast perception in elephants given their arrhythmic lifestyle.