Headbutting through time: A review of this hypothesized behavior in "dome-headed" fossil taxa.

Headbutting is a combative behavior most popularly portrayed and exemplified in the extant bighorn sheep (Ovis canadensis). When behaviorally proposed in extinct taxa, these organisms are oft depicted Ovis-like as having used modified cranial structures to combatively slam into one another. The combative behavioral hypothesis of headbutting has a long and rich history in the vertebrate fossil literature (not just within Dinosauria), but the core of this behavioral hypothesis in fossil terrestrial vertebrates is associated with an enlarged osseous cranial dome-an osteological structure with essentially no current counterpart. One confounding issue found in the literature is that while the term "headbutting" sounds simplistic enough, little terminology has been used to describe this hypothesized behavior. And pertinent to this special issue, potential brain trauma and the merits of such proposed pugilism have been assessed largely from the potential deformation of the overlying osseous structure; despite the fact that extant taxa readily show that brain damage can and does occur without osteological compromise. Additionally, the extant taxa serving as the behavioral counterpart for comparison are critical, not only because of the combative behaviors and morphologies they display, but also the way they engage in such behavior. Sheep (Ovis), warthogs (Phacochoerus), and bison (Bison) all engage in various forms of "headbutting", but the cranial morphologies and the way each engages in combat is markedly different. To hypothesize that an extinct organism engaged in headbutting like an extant counterpart in theory implies specific striking:contacting surfaces, speed, velocity, and overall how that action was executed. This review examines the history and usage of the headbutting behavioral hypothesis in these dome-headed fossil taxa, their respective extant behavioral counterparts, and proposes a protocol for specific behavioral terms relating to headbutting to stem future confusion. We also discuss the disparate morphology of combative cranial structures in the fossil record, and the implications of headbutting-induced brain injury in extinct taxa. Finally, we conclude with some potential implications for artistic reconstructions of fossil taxa regarding this behavioral repertoire.

Neurobiological tradeoffs of headbutting bovids.

Bovids are notorious for their high-force headbutting fights for herd dominance. Here, I discuss the evolutionary tradeoff between headbutting and brain damage incurred by bovids' reproductive strategy. The specific behavioral and neuroanatomical adaptations of these animals are placed in context of the neuropathology of repetitive brain trauma.

Evidence of traumatic brain injury in headbutting bovids.

Traumatic brain injury (TBI) is a leading cause of neurologic impairment and death that remains poorly understood. Rodent models have yet to produce clinical therapies, and the exploration of larger and more diverse models remains relatively scarce. We investigated the potential for brain injury after headbutting in two combative bovid species by assessing neuromorphology and neuropathology through immunohistochemistry and stereological quantification. Postmortem brains of muskoxen (Ovibos moschatus, n = 3) and bighorn sheep (Ovis canadensis, n = 4) were analyzed by high-resolution MRI and processed histologically for evidence of TBI. Exploratory histological protocols investigated potential abnormalities in neurons, microglia, and astrocytes in the prefrontal and parietal cortex. Phosphorylated tau protein, a TBI biomarker found in the cerebrospinal fluid and in neurodegenerative lesions, was used to detect possible cellular consequences of chronic or acute TBI. MRI revealed no abnormal neuropathological changes; however, high amounts of tau-immunoreactive neuritic thread clusters, neurites, and neurons were concentrated in the superficial layers of the neocortex, preferentially at the bottom of the sulci in the muskoxen and occasionally around blood vessels. Tau-immunoreactive lesions were rare in the bighorn sheep. Additionally, microglia and astrocytes showed no grouping around tau-immunoreactive cells in either species. Our preliminary findings indicate that muskoxen and possibly other headbutting bovids suffer from chronic or acute brain trauma and that the males' thicker skulls may protect them to a certain extent.

Macrowear effects of external quartz abrasives of different size and concentration in rabbits (Oryctolagus cuniculus).

External quartz abrasives are one of the driving forces of macrowear in herbivorous animals. We tested to what extent different sizes and concentrations influence their effect on tooth wear. We fed seven pelleted diets varying only in quartz concentration (0%, 4%, and 8%) and size (fine silt: ∼4 µm, coarse silt: ∼50 µm, fine sand: ∼130 µm) to rabbits (Oryctolagus cuniculus, n = 16) for 2 weeks each in a randomized serial experiment. Measurements to quantify wear and growth of incisors and the mandibular first cheek tooth, as well as heights of all other cheek teeth, were performed using calipers, endoscopic examination, and computed tomography scans before and after each feeding period. Tooth growth showed a compensatory correlation with wear. Absolute tooth height (ATH) and relative tooth height (RTH); relative to the 0% quartz "control" diet) was generally lower on the higher concentration and the larger size of abrasives. The effect was more pronounced on the maxillary teeth, on specific tooth positions and the right jaw side. When offered the choice between different sizes of abrasives, the rabbits favored the silt diets over the control and the fine sand diet; in a second choice experiment with different diets, they selected a pelleted diet with coarse-grained sand, however. This study confirms the dose- and size-dependent wear effects of external abrasives, and that hypselodont teeth show compensatory growth. The avoidance of wear did not seem a priority for animals with hypselodont teeth, since the rabbits did not avoid diets inducing a certain degree of wear.

Tooth wear, growth and height in rabbits (Oryctolagus cuniculus) fed pelleted or extruded diets with or without added abrasives.

Among the different factors thought to affect dental wear, dietary consistency is possibly the least investigated. To understand tooth wear of herbivorous animals consuming different dietary consistencies with different abrasive potential, we fed 14 rabbits (Oryctolagus cuniculus) exclusively with a timothy grassmeal-based diet in either pelleted or extruded form, or the same diets with an addition of 5% fine sand abrasives (mean size 130 µm). First, we offered the rabbits the pelleted and extruded diets as well as the pelleted control and pelleted abrasive diet in a two-stage preference experiment. Then, the rabbits received each diet for 2 weeks in a randomised serial feeding experiment, where each animal served as its own control. Tooth measurements for wear, growth and height were achieved using a manual calliper, endoscopic examination and CT scans. The analysis of the diets as fed showed almost identical mean particle size, but the extruded diet had a lower density (volume/mass) and softer consistency compared to the pelleted one and was favoured by most rabbits. The rabbits selected against the diet with sand during the preference experiment, possibly because it caused more tooth wear, especially on the teeth most exposed to wear along the upper tooth row (upper P4 and M1). The maxillary teeth also showed evidence of an increased chewing laterality by the end of the experiment. The extruded diet led to a significantly lower cheek teeth height than the pelleted diet, potentially due to the higher chewing effort needed for a similar dry matter intake. The results suggest that dietary hardness alone is a poor predictor of dental wear. The regrowth of the teeth matched wear consistently.

Dental wear proxy correlation in a long-term feeding experiment on sheep (Ovis aries).

Dietary reconstruction in vertebrates often relies on dental wear-based proxies. Although these proxies are widely applied, the contributions of physical and mechanical processes leading to meso- and microwear are still unclear. We tested their correlation using sheep (Ovis aries, n = 39) fed diets of varying abrasiveness for 17 months as a model. Volumetric crown tissue loss, mesowear change and dental microwear texture analysis (DMTA) were all applied to the same teeth. We hereby correlate: (i) 46 DMTA parameters with each other, for the maxillary molars (M1, M2, M3), and the second mandibular molar (m2); (ii) 10 mesowear variables to each other and to DMTA for M1, M2, M3 and m2; and (iii) volumetric crown tissue loss to mesowear and DMTA for M2. As expected, many DMTA parameters correlated strongly with each other, supporting the application of reduced parameter sets in future studies. Correlation results showed only few DMTA parameters correlated with volumetric tissue change and even less so with mesowear variables, with no correlation between mesowear and volumetric tissue change. These findings caution against interpreting DMTA and mesowear patterns in terms of actual tissue removal until these dental wear processes can be better understood at microscopic and macroscopic levels.

Unconventional animal models for traumatic brain injury and chronic traumatic encephalopathy.

Traumatic brain injury (TBI) is one of the main causes of death worldwide. It is a complex injury that influences cellular physiology, causes neuronal cell death, and affects molecular pathways in the brain. This in turn can result in sensory, motor, and behavioral alterations that deeply impact the quality of life. Repetitive mild TBI can progress into chronic traumatic encephalopathy (CTE), a neurodegenerative condition linked to severe behavioral changes. While current animal models of TBI and CTE such as rodents, are useful to explore affected pathways, clinical findings therein have rarely translated into clinical applications, possibly because of the many morphofunctional differences between the model animals and humans. It is therefore important to complement these studies with alternative animal models that may better replicate the individuality of human TBI. Comparative studies in animals with naturally evolved brain protection such as bighorn sheep, woodpeckers, and whales, may provide preventive applications in humans. The advantages of an in-depth study of these unconventional animals are threefold. First, to increase knowledge of the often-understudied species in question; second, to improve common animal models based on the study of their extreme counterparts; and finally, to tap into a source of biological inspiration for comparative studies and translational applications in humans.

Aging: What We Can Learn From Elephants.

Elephants are large-brained, social mammals with a long lifespan. Studies of elephants can provide insight into the aging process, which may be relevant to understanding diseases that affect elderly humans because of their shared characteristics that have arisen through independent evolution. Elephants become sexually mature at 12 to 14 years of age and are known to live into, and past, their 7th decade of life. Because of their relatively long lifespans, elephants may have evolved mechanisms to counter age-associated morbidities, such as cancer and cognitive decline. Elephants rely heavily on their memory, and engage in multiple levels of competitive and collaborative relationships because they live in a fission-fusion system. Female matrilineal relatives and dependent offspring form tight family units led by an older-aged matriarch, who serves as the primary repository for social and ecological knowledge in the herd. Similar to humans, elephants demonstrate a dependence on social bonds, memory, and cognition to navigate their environment, behaviors that might be associated with specializations of brain anatomy. Compared with other mammals, the elephant hippocampus is proportionally smaller, whereas the temporal lobe is disproportionately large and expands laterally. The elephant cerebellum is also relatively enlarged, and the cerebral cortex is highly convoluted with numerous gyral folds, more than in humans. Last, an interesting characteristic unique to elephants is the presence of at least 20 copies of the TP53 tumor suppressor gene. Humans have only a single copy. TP53 encodes for the p53 protein, which is known to orchestrate cellular response to DNA damage. The effects of these multiple copies of TP53 are still being investigated, but it may be to protect elephants against multiple age-related diseases. For these reasons, among others, studies of elephants would be highly informative for aging research. Elephants present an underappreciated opportunity to explore further common principles of aging in a large-brained mammal with extended longevity. Such research can contribute to contextualizing our knowledge of age-associated morbidities in humans.

Confirmation of a wear-compensation mechanism in dental roots of ruminants.

Diet affects many factors of an animal's anatomy, but teeth are a specific focus of dietary research, as their durability lends them to record information on a large variety of scales. Abrasive diets like those of grazing herbivores are known to wear down teeth, but how that wear affects tooth growth and the relations between its different morphological components is rarely investigated. Seven pelleted diets varying in abrasive size and concentration were fed over a 17-month period to 49 sheep (Ovis aries), of which n = 39 qualified for morphology measurements. Using computed tomography, scans of the skulls were made over the course of the experiment, and the impact of diet-related wear was observed on tooth volume and morphology, including the position of dental burr marks, over time. Digital caliper measurements were applied to 3D renderings of the teeth, and the volume of crown and root segments were investigated separately. We aimed to detect a signal of root growth compensating for wear, and test if this mechanism would be affected by dietary abrasives. Crown-segment volume loss was correlated to root-segment volume gain. Height and burr mark measurements indicated a much higher experimental tooth wear than that previously reported for free-ranging animals. The reason for this is unclear. There was no relationship between tooth height and dentine basin depth. For all parameters, there was no effect of diet; hence, while the measurements corroborate general understanding of tooth wear and compensatory processes, these methods appear not suitable to assess subtle differences between feeding regimes.

Intraspecific macroscopic digestive anatomy of ring-tailed lemurs (Lemur catta), including a comparison of frozen and formalin-stored specimens.

Digestive tract measurements are often considered species specific, but little information exists on the degree to which they change during ontogeny within a species. Additionally, access to anatomical material from nondomestic species is often limited, with fixed tissues possibly representing the only available source, though the degree to which this material is representative in terms of dimensions and weight is debatable. In the present study, the macroscopic anatomy of the digestive tract (length of intestinal sections, and tissue weights of stomach and intestines) of 58 Lemur catta [ranging in age from 1 month (neonates) to 25 years], which had been stored frozen (n = 27) or fixed in formalin (n = 31), was quantified. Particular attention was paid to the caecum and the possible presence of an appendix. The intraspecific allometric scaling of body mass (BM)0.46[0.40;0.51] for total intestine length and BM0.48[0.41;0.54] for small intestine length was higher than the expected geometric scaling of BM0.33, and similar to that reported in the literature for interspecific scaling. This difference in scaling is usually explained by the hypothesis that, to maintain optimal absorption, the diameter of the intestinal tube cannot increase geometrically. Therefore, geometric volume gain of increasing body mass is accommodated for by more-than-geometric length scaling. According to the literature, not all L. catta have an appendix. No appendix was found in the specimens in the present study. The proportions of length measurements did not change markedly during ontogeny, indicating that the proportions of the foetus are representative of those of the adult animal. By contrast, width and tissue-mass scaling of the caecum indicated disproportionate growth of this organ during ontogeny that was not reflected in its length. Compared to overall intraspecific variation, the method of storage (frozen vs. formalin) had no relevant impact on length or weight measurements.

The history of mesowear: a review.

Published mesowear data was reviewed from the year 2000 to November 2019 (211 publications, 707 species, 1,396 data points). Mesowear is a widely applied tooth wear technique that can be used to infer a herbivore's diet by scoring the height and sharpness of molar tooth cusps with the naked eye. Established as a fast and efficient tool for paleodiet reconstruction, the technique has seen multiple adaptations, simplifications, and extensions since its establishment, which have become complex to follow. The present study reviews all successive changes and adaptations to the mesowear technique in detail, providing a template for the application of each technique to the research question at hand. In addition, the array of species to which mesowear has been applied, along with the equivalent recorded diets have been compiled here in a large dataset. This review provides an insight into the metrics related to mesowear publication since its establishment. The large dataset overviews whether the species to which the various techniques of mesowear are applied are extant or extinct, their phylogenetic classification, their assigned diets and diet stability between studies, as a resource for future research on the topic.

Dust and grit matter: abrasives of different size lead to opposing dental microwear textures in experimentally fed sheep (Ovis aries).

External abrasives ingested along with the herbivore diet are considered main contributors to dental wear, though how the different sizes and concentrations of these abrasives influence wear remains unclear. Dental microwear texture analysis (DMTA) is an established method for dietary reconstruction which describes a tooth's surface topography on a micrometre scale. The method has yielded conflicting results as to the effect of external abrasives. In the present study, a feeding experiment was performed on sheep (Ovis aries) fed seven diets of different abrasiveness. Our aim was to discern the individual effects of size (4, 50 and 130 µm) and concentration (0%, 4% and 8% of dry matter) of abrasives on dental wear, applying DMTA to four tooth positions. Microwear textures differed between individual teeth, but surprisingly, showed no gradient along the molar tooth row, and the strongest differentiation of experimental groups was achieved when combining data of all maxillary molars. Overall, a pattern of increasing height, volume and complexity of the tooth's microscopic surface appeared with increasing size of dietary abrasives, and when compared with the control, the small abrasive diets showed a polishing effect. The results indicate that the size of dietary abrasives is more important for dental microwear texture traces than their concentration, and that different sizes can have opposing effects on the dietary signal. The latter finding possibly explains conflicting evidence from previous experimental DMTA applications. Further exploration is required to understand whether and how microscopic traces created by abrasives translate quantitatively to tissue loss.

Root growth compensates for molar wear in adult goats (Capra aegagrus hircus).

One reason for the mammalian clade's success is the evolutionary diversity of their teeth. In herbivores, this is represented by high-crowned teeth evolved to compensate for wear caused by dietary abrasives like phytoliths and grit. Exactly how dietary abrasives wear teeth is still not understood completely. We fed four different pelleted diets of increasing abrasiveness (L: Lucerne; G: grass; GR: grass and rice husks; GRS: grass, rice husks, and sand) to four groups of a total of 28 adult goats, all with completely erupted third molars, over a six-month period. Tooth morphology was captured by medical computed tomography scans at the beginning and end of the controlled feeding experiment, and separation lines between the crown and root segments were defined in the upper right second molar (M2), to gauge absolute wear. Using bootstrapping, significant differences in volume loss between diets L/G and GR/GRS were detected. A small but nevertheless consistent volume gain was noted in the roots, and there was a significant, positive correlation between crown volume loss and root volume gain. This growth could possibly be attributed to the well-known process of cementum deposition and its relation with a putative feedback mechanism, in place to attenuate wear caused by abrasive diets.

Controlled feeding experiments with diets of different abrasiveness reveal slow development of mesowear signal in goats (Capra aegagrus hircus).

Dental mesowear is applied as a proxy to determine the general diet of mammalian herbivores based on tooth-cusp shape and occlusal relief. Low, blunt cusps are considered typical of grazers and high, sharp cusps typical of browsers. However, how internal or external abrasives impact mesowear, and the time frame the wear signature takes to develop, still need to be explored. Four different pelleted diets of increasing abrasiveness (lucerne, grass, grass and rice husks, and grass, rice husks and sand) were fed to four groups of a total of 28 adult goats in a controlled feeding experiment over a 6-month period. Tooth morphology was captured by medical CT scans at the beginning and end of the experiment. These scans, as well as the crania obtained post mortem, were scored using the mesowear method. Comparisons between diet groups showed few significant differences after 6 months, irrespective of whether CT scans or the real teeth were scored. Only when assessing the difference in signal between the beginning and the end of the experiment did relevant, significant diet-specific effects emerge. Diets containing lower phytolith content caused a more pronounced change in mesowear towards sharper cusps/higher reliefs, while the feed containing sand did not result in more extreme changes in mesowear when compared with the same feed without sand. Our experiment suggests that the formation of a stable and hence reliable mesowear signal requires more time to develop than 6 months.