Describing whisker morphology of the Carnivora.

One of the largest ecological transitions in carnivoran evolution was the shift from terrestrial to aquatic lifestyles, which has driven morphological diversity in skulls and other skeletal structures. In this paper, we investigate the association between those lifestyles and whisker morphology. However, comparing whisker morphology over a range of species is challenging since the number of whiskers and their positions on the mystacial pads vary between species. Also, each whisker will be at a different stage of growth and may have incurred damage due to wear and tear. Identifying a way to easily capture whisker morphology in a small number of whisker samples would be beneficial. Here, we describe individual and species variation in whisker morphology from two-dimensional scans in red fox, European otter and grey seal. A comparison of long, caudal whiskers shows inter-species differences most clearly. We go on to describe global whisker shape in 24 species of carnivorans, using linear approximations of curvature and taper, as well as traditional morphometric methods. We also qualitatively examine surface texture, or the presence of scales, using scanning electron micrographs. We show that gross whisker shape is highly conserved, with whisker curvature and taper obeying simple linear relationships with length. However, measures of whisker base radius, length, and maybe even curvature, can vary between species and substrate preferences. Specifically, the aquatic species in our sample have thicker, shorter whiskers that are smoother, with less scales present than those of terrestrial species. We suggest that these thicker whiskers may be stiffer and able to maintain their shape and position during underwater sensing, but being stiffer may also increase wear.

Demonstrating a measurement protocol for studying comparative whisker movements with implications for the evolution of behaviour.

BACKGROUND: Studying natural, complex behaviours over a range of different species provides insights into the evolution of the brain and behaviour. Whisker movements reveal complex behaviours; however, there does not yet exist a protocol that is able to capture whisker movements and behaviours in a range of different species. NEW METHOD: We develop a new protocol and make recommendations for measuring comparative whisker movements and behaviours. Using two set-ups - an enclosure camera set-up and a high-speed video set-up - we capture and measure the whisker movements of sixteen different captive mammal species from four different animal collections. RESULTS: We demonstrate the ability to describe whisker movements and behaviours across a wide range of mammalian species. We describe whisker movements in European hedgehog, Cape porcupine, domestic rabbit, domestic ferret, weasel, European otter and red fox for the first time. We observe whisker movements in all the species we tested, although movement, positions and behaviours vary in a species-specific way. COMPARISON WITH EXISTING METHOD(S): The high-speed video set-up is based on the protocols of previous studies. The addition of an enclosure video set-up is entirely new, and allows us to include more species, especially large and shy species that cannot be moved into a high-speed filming arena. CONCLUSIONS: We make recommendations for comparative whisker behaviour studies, particularly incorporating individual and species-specific considerations. We believe that flexible, comparative behavioural protocols have wide-ranging applications, specifically to better understand links between the brain and complex behaviours.

The evolutionary origin of avian facial bristles and the likely role of rictal bristles in feeding ecology.

Facial bristles are one of the least described feather types and have not yet been systematically studied across phylogenetically diverse avian species. Consequently, little is known about their form, function and evolutionary history. Here we address this knowledge gap by characterising the evolution of facial bristles for the first time. We especially focus on rictal bristle presence and their associations with foraging behaviour, diet and habitat preferences in 1022 avian species, representing 91 families in 29 orders. Results reveal that upper rictal, lower rictal and interramal bristles were likely to be present in the most recent common ancestor of this avian phylogeny, whereas narial bristles were likely to be absent. Rictal bristle presence, length and shape varied both within and between avian orders, families and genera. Rictal bristles were gained or lost multiple times throughout evolution, which suggest that the different morphologies observed within species might not be homologous. Phylogenetic relatedness is also not likely to be the only driver of rictal bristle presence and morphology. Rictal bristle presence and length were associated with species-specific ecological traits, especially nocturnality. Our findings suggest that species foraging in low-light conditions are likely to have longer rictal bristles, and that rictal bristles are likely to have evolved in early birds.

Abnormal whisker movements in the 3xTg-AD mouse model of Alzheimer's disease.

Alzheimer's disease is the most frequent form of dementia in elderly people. The triple transgenic (3xTg-AD) mouse model of Alzheimer's Disease is important in biomedical research as these mice develop both neuropathological and behavioural phenotypes. However, their behavioural phenotype is variable, with findings depending on the specific task, as well as the age and sex of the mice. Whisker movements show motor, sensory and cognitive deficits in mouse models of neurodegenerative disease. Therefore, we examined whisker movements in 3, 12.5 and 17-month-old female 3xTg-AD mice and their B6129S/F2 wildtype controls. Mice were filmed using a high-speed video camera (500 fps) in an open arena during a novel object exploration task. Genotype and age differences were found in mice exploring the arena prior to object contact. Prior to whisker contact, the 3-month-old 3xTg-AD mice had smaller whisker angles compared with the wildtype controls, suggesting an early motor phenotype in these mice. Pre-contact mean angular position at 3 months and whisking amplitude at 17 months of age differed between the 3xTg-AD and wildtype mice. During object contact 3xTg-AD mice did not reduce whisker spread as frequently as the wildtype mice at 12.5 and 17 months, which may suggest sensory or attentional deficits. We show that whisker movements are a powerful behavioural measurement tool for capturing behavioural deficits in mouse models that show complex phenotypes, such as the 3xTg-AD mouse model.

A Review and Case Study of 3D Imaging Modalities for Female Amniote Reproductive Anatomy.

Recent advances in non-invasive imaging methods have revitalised the field of comparative anatomy, and reproductive anatomy has been no exception. The reproductive systems of female amniotes present specific challenges, namely their often internal "hidden" anatomy. Quantifying female reproductive systems is crucial to recognising reproductive pathologies, monitoring menstrual cycles, and understanding copulatory mechanics. Here we conduct a review of the application of non-invasive imaging techniques to female amniote reproductive anatomy. We introduce the commonly used imaging modalities of computed tomography (CT) and magnetic resonance imaging (MRI), highlighting their advantages and limitations when applied to female reproductive tissues, and make suggestions for future advances. We also include a case study of micro CT and MRI, along with their associated staining protocols, applied to cadavers of female adult stoats (Mustela erminea). In doing so, we will progress the discussion surrounding the imaging of female reproductive anatomy, whilst also impacting the fields of sexual selection research and comparative anatomy more broadly.

Morphological peculiarities of a harbour seal (Phoca vitulina) whisker revealed by normal skeletonisation.

Of all mammalian vibrissae, those of certain species of pinnipeds are exceptional. Researchers believe that their curious undulating form evolved for hydrodynamic detection. Our understanding of how these whiskers work depends on a geometrical model that captures the crucial pertinent features of the natural vibrissae including its tapering and curvature. It should also account for the form of the whisker when it flexes under external loading. We introduce and study a normal skeleton of a two-dimensional projection of a harbour seal whisker. The normal skeleton is a complete shape descriptor that involves reduction to the centreline equipped with a thickness function of the orthogonal cross-section. The contours of the whisker shape are extracted from a 2D greyscale scan. Our analysis reveals correspondence between the undulations of the width and oscillations of the centreline curvature as functions of arc length. We discuss two possible explanations for that remarkable feature: one based on consideration of growth and the other of plastic deformation. For the latter we employ a mechanical model to demonstrate appearance of curvature oscillations caused by extensive deflection of the undulating whisker due to external loading.

Anatomy of bristles on the nares and rictus of western barn owls (Tyto alba).

Many nocturnal avian species, such as Strigiformes, Caprimulgiformes and Apterygiformes, have sensitive vibrotactile bristles on their upper bill, especially on their rictus. The anatomy of these bristles can vary, especially in terms of sensitivity (Herbst corpuscle number), bristle length and bristle number. This variation is thought to be associated with foraging - such that diurnal, open foragers have smaller and less-sensitive bristles. Here, we describe bristle morphology and follicle anatomy in the western barn owl (Tyto alba) for the first time, using both live and roadkill wild owls. We show that T. alba have both narial and rictal bristles that are likely to be vibrotactile, since they have Herbst corpuscles around their follicles. We observed more numerous (~8) and longer bristles (~16 mm) on the nares of T. alba, than on the rictal region (~4 and ~13 mm respectively). However, the narial bristle follicles contained fewer Herbst corpuscles in their surroundings (~5) than the rictal bristles (~7); indicating that bristle length is not indicative of sensitivity. As well as bristle length and number varying between different facial regions, they also varied between individuals, although the cause of this variation remains unclear. Despite this variation, the gross anatomy of facial bristle follicles appears to be conserved between nocturnal Strigiformes, Caprimulgiformes and Apterygiformes. Understanding more about how T. alba use their bristles would, therefore, give us greater insights into the function of avian bristles in general.

Morphometrics for sports mechanics: Showcasing tennis racket shape diversity.

Tennis racket design has changed from its conception in 1874. While we know that modern tennis rackets are lighter and have larger heads than their wooden predecessors, it is unknown how their gross shape has changed specifically. It is also unknown how racket shape is related to factors that influence performance, like the Transverse and Polar moments of inertia. The aim of this study was to quantify how tennis racket shape has changed over time, with a view to furthering our understanding of how such developments have influenced the game. Two-dimensional morphometric analysis was applied to silhouettes extracted from photographs of 514 rackets dating from 1874 to 2017. A principal component analysis was conducted on silhouette outlines, to allow racket shape to be summarised. The rackets were grouped by age and material for further analysis. Principal Component 1 accounted for 87% of the variation in racket shape. A pairwise Pearson's correlation test indicated that head width and length were both strongly correlated to Principal Component 1 (r = 0.916 & r = 0.801, p-values<0.001). Principal Component 1 was also correlated to the Polar (r = 0.862, p<0.001) and Transverse (r = -0.506, p<0.001) moments of inertia. Racket age and material had a medium (p<0.001, η2p = 0.074) and small (p = 0.015, η2p = 0.017) effect on Principal Component 1, respectively. Mean racket shapes were also generated from the morphometric analyses for the material and age groupings, and we consider how these shape changes may have influenced performance and injury risk. These mean shape groupings could support the development of models, such as finite element analysis, for predicting how historical developments in tennis equipment have affected performance and injury risk.

Comparing vibrissal morphology and infraorbital foramen area in pinnipeds.

Pinniped vibrissae are well-adapted to sensing in an aquatic environment, by being morphologically diverse and more sensitive than those of terrestrial species. However, it is both challenging and time-consuming to measure vibrissal sensitivity in many species. In terrestrial species, the infraorbital foramen (IOF) area is associated with vibrissal sensitivity and increases with vibrissal number. While pinnipeds are thought to have large IOF areas, this has not yet been systematically measured before. We investigated vibrissal morphology, IOF area, and skull size in 16 species of pinniped and 12 terrestrial Carnivora species. Pinnipeds had significantly larger skulls and IOF areas, longer vibrissae, and fewer vibrissae than the other Carnivora species. IOF area and vibrissal number were correlated in Pinnipeds, just as they are in terrestrial mammals. However, despite pinnipeds having significantly fewer vibrissae than other Carnivora species, their IOF area was not smaller, which might be due to pinnipeds having vibrissae that are innervated more. We propose that investigating normalized IOF area per vibrissa will offer an alternative way to approximate gross individual vibrissal sensitivity in pinnipeds and other mammalian species. Our data show that many species of pinniped, and some species of felids, are likely to have strongly innervated individual vibrissae, since they have high values of normalized IOF area per vibrissa. We suggest that species that hunt moving prey items in the dark will have more sensitive and specialized vibrissae, especially as they have to integrate between individual vibrissal signals to calculate the direction of moving prey during hunting.

Diversity of vibrissal follicle anatomy in cetaceans.

Most cetaceans are born with vibrissae but they can be lost or reduced in adulthood, especially in odontocetes. Despite this, some species of odontocetes have been found to have functioning vibrissal follicles (including the follicle itself and any remaining vibrissal hair shaft) that play a role in mechanoreception, proprioception and electroreception. This reveals a greater diversity of vibrissal function in odontocetes than in any other mammalian group. However, we know very little about vibrissal follicle form and function across the Cetacea. Here, we qualitatively describe the gross vibrissal follicle anatomy of fetuses of three species of cetaceans, including two odontocetes: Atlantic white-sided dolphin (Lagenorhynchus acutus), harbour porpoise (Phocoena phocoena), and one mysticete: minke whale (Balaenoptera acutorostrata), and compared our findings to previous anatomical descriptions. All three species had few, short vibrissae contained within a relatively simple, single-part follicle, lacking in muscles. However, we observed differences in vibrissal number, follicle size and shape, and innervation distribution between the species. While all three species had nerve fibers around the follicles, the vibrissal follicles of Balaenoptera acutorostrata were innervated by a deep vibrissal nerve, and the nerve fibers of the odontocetes studied were looser and more branched. For example, in Lagenorhynchus acutus, branches of nerve fibers travelled parallel to the follicle, and innervated more superficial areas, rather than just the base. Our anatomical descriptions lend support to the observation that vibrissal morphology is diverse in cetaceans, and is worth further investigation to fully explore links between form and function.

Investigating Foot Morphology in Rock Climbing Mammals: Inspiration for Biomimetic Climbing Shoes.

The sporting goods sector can serve as a proving ground for new technologies. We propose that climbing shoes are an excellent case study for showcasing a systematic approach to bio-inspired design. Foot adaptations to climbing have been described before in some animals and have even been incorporated into bio-inspired products. However, there has not yet been a systematic description of climbing adaptations in mammals, and especially in rock climbing species. We present a description of foot morphology in mammals and compare rock climbing species to those with other locomotion types. Our results show that rock climbing species in our sample had fewer digits and larger anterior pads than arboreal species. Rock climbing species often had hooves or, if they had foot pads, these were relatively smooth. These examples look a bit like current climbing shoe designs, perhaps suggesting convergent evolution. However, there was also variation, with rock climbing species having pads varying in shape, placement and texture. Much of this variation is likely to be dependent on the relatedness of species, with those that are more related having more similar feet. We suggest that incorporation of novel textures and compliant pads might be an interesting focus for future climbing shoe designs.

California sea lions employ task-specific strategies for active touch sensing.

Active sensing is the process of moving sensors to extract task-specific information. Whisker touch is often referred to as an active sensory system as whiskers are moved with purposeful control. Even though whisker movements are found in many species, it is unknown whether any animal can make task-specific movements with their whiskers. California sea lions (Zalophus californianus) make large, purposeful whisker movements and are capable of performing many whisker-related discrimination tasks. Therefore, California sea lions are an ideal species to explore the active nature of whisker touch sensing. Here, we show that California sea lions can make task-specific whisker movements. California sea lions move their whiskers with large amplitudes around object edges to judge size, make smaller, lateral stroking movements to judge texture and make very small whisker movements during a visual task. These findings, combined with the ease of training mammals and measuring whisker movements, makes whiskers an ideal system for studying mammalian perception, cognition and motor control.

Investigating cat predation as the cause of bat wing tears using forensic DNA analysis.

Cat predation upon bat species has been reported to have significant effects on bat populations in both rural and urban areas. The majority of research in this area has focussed on observational data from bat rehabilitators documenting injuries, and cat owners, when domestic cats present prey. However, this has the potential to underestimate the number of bats killed or injured by cats. Here, we use forensic DNA analysis techniques to analyze swabs taken from injured bats in the United Kingdom, mainly including Pipistrellus pipistrellus (40 out of 72 specimens). Using quantitative PCR, cat DNA was found in two-thirds of samples submitted by bat rehabilitators. Of these samples, short tandem repeat analysis produced partial DNA profiles for approximately one-third of samples, which could be used to link predation events to individual cats. The use of genetic analysis can complement observational data and potentially provide additional information to give a more accurate estimation of cat predation.

Ecomorphology reveals Euler spiral of mammalian whiskers.

Whiskers are present in many species of mammals. They are specialised vibrotactile sensors that sit within strongly innervated follicles. Whisker size and shape will affect the mechanical signals that reach the follicle, and hence the information that reaches the brain. However, whisker size and shape have not been quantified across mammals before. Using a novel method for describing whisker curvature, this study quantifies whisker size and shape across 19 mammalian species. We find that gross two-dimensional whisker shape is relatively conserved across mammals. Indeed, whiskers are all curved, tapered rods that can be summarised by Euler spiral models of curvature and linear models of taper, which has implications for whisker growth and function. We also observe that aquatic and semi-aquatic mammals have relatively thicker, stiffer, and more highly tapered whiskers than arboreal and terrestrial species. In addition, smaller mammals tend to have relatively long, slender, flexible whiskers compared to larger species. Therefore, we propose that whisker morphology varies between larger aquatic species, and smaller scansorial species. These two whisker morphotypes are likely to induce quite different mechanical signals in the follicle, which has implications for follicle anatomy as well as whisker function.

Anatomy of avian rictal bristles in Caprimulgiformes reveals reduced tactile function in open-habitat, partially diurnal foraging species.

Avian rictal bristles are present in many species of birds, especially in nocturnal species. Rictal bristles occur along the upper beak and are morphologically similar to mammalian whiskers. Mammalian whiskers are important tactile sensors, guiding locomotion, foraging and social interactions, and have a well-characterised anatomy. However, it is not yet known whether avian rictal bristles have a sensory function, and their morphology, anatomy and function have also not been described in many species. Our study compares bristle morphology, follicle anatomy and their association with foraging traits, across 12 Caprimulgiform species. Rictal bristle morphology and follicle anatomy were diverse across the 12 species. Nine of the 12 species had mechanoreceptors around their bristle follicles; however, there was large variation in their musculature, mechanoreceptor numbers and bristle morphology. Overall, species with short, thin, branching bristles that lacked mechanoreceptors tended to forage pre-dusk in open habitats, whereas species with mechanoreceptors around their bristle follicle tended to forage at night and in more closed habitats. We suggest that rictal bristles are likely to be tactile in many species and may aid in navigation, foraging and collision avoidance; however, identifying rictal bristle function is challenging and demands further investigation in many species.

Pinnipeds orient and control their whiskers: a study on Pacific walrus, California sea lion and Harbor seal.

Whisker touch is an active sensory system. Previous studies in Pinnipeds have adopted relatively stationary tasks to judge tactile sensitivity, which may not accurately promote natural whisker movements and behaviours. This study developed a novel feeding task, termed fish sweeping to encourage whisker movements. Head and whisker movements were tracked from video footage in Harbor seal (Phoca vitulina), California sea lion (Zalophus californianus) and Pacific walrus (Odobenus rosmarus divergens). All species oriented their head towards the moving fish target and moved their whiskers during the task. Some species also engaged in whisker control behaviours, including head-turning asymmetry in the Pacific walrus, and contact-induced asymmetry in the Pacific walrus and California sea lion: behaviours that have only previously been observed in terrestrial mammals. This study confirms that Pinnipeds should be thought of as whisker specialists, and that whisker control (movement and positioning) is an important aspect of touch sensing in these animals, especially in sea lions and walruses. That the California sea lion controls whisker movement in relation to an object, and also had large values of whisker amplitude, spread and asymmetry, suggests that California sea lions are a promising model with which to further explore active touch sensing.

The Euler spiral of rat whiskers.

This paper reports on an analytical study of the intrinsic shapes of 523 whiskers from 15 rats. We show that the variety of whiskers on a rat's cheek, each of which has different lengths and shapes, can be described by a simple mathematical equation such that each whisker is represented as an interval on the Euler spiral. When all the representative curves of mystacial vibrissae for a single rat are assembled together, they span an interval extending from one coiled domain of the Euler spiral to the other. We additionally find that each whisker makes nearly the same angle of 47∘ with the normal to the spherical virtual surface formed by the tips of whiskers, which constitutes the rat's tactile sensory shroud or "search space." The implications of the linear curvature model for gaining insight into relationships between growth, form, and function are discussed.

Whisker exploration behaviours in the 5xFAD mouse are affected by sex and retinal degeneration.

Active whisking in mice and rats is one of the fastest behaviours known in mammals and is used to guide complex behaviours such as exploration and navigation. During object contact, whisker movements are actively controlled and undergo robust changes in timing, speed and position. This study quantifies whisker movements in 6- to 7-month old male and female 5xFAD mice, and their C57/SJL F1 wild-type (WT) controls. As well as genotype, we examined sex differences and the effects of retinal degeneration (rd). Mice were filmed using a high-speed video camera at 500 frames per second (fps), under infrared light while behaving freely in three tasks: object exploration, sequential object exploration and tunnel running. Measures of whisker position, amplitude, speed and asymmetry were extracted and analysed for each task. The 5xFAD mice had significantly altered whisker angular positions, amplitude and asymmetry during object contacts and female 5xFAD mice with rd had lower mean angular positions during object contact. There were no significant effects of genotype on sequential object exploration or on tunnel running but differences due to sex and rd were found in both tasks, with female mice making larger and faster whisker movements overall, and mice with rd making larger and faster whisker movements during object contact. There were sex differences in whisker movements during sequential object exploration and females with rd had higher whisker retraction speeds in tunnel running. These data show that measuring whisker movements can quantify genotype and sex differences and the effects of rd during exploratory behaviour in these mice.

Good Vibrations: The Evolution of Whisking in Small Mammals.

While most mammals have whiskers, some tactile specialists-mainly small, nocturnal, and arboreal species-can actively move their whiskers in a symmetrical, cyclic movement called whisking. Whisking enables mammals to rapidly, tactually scan their environment to efficiently guide locomotion and foraging in complex habitats. The muscle architecture that enables whisking is preserved from marsupials to primates, prompting researchers to suggest that a common ancestor might have had moveable whiskers. Studying the evolution of whisker touch sensing is difficult, and we suggest that measuring an aspect of skull morphology that correlates with whisking would enable comparisons between extinct and extant mammals. We find that whisking mammals have larger infraorbital foramen (IOF) areas, which indicates larger infraorbital nerves and an increase in sensory acuity. While this relationship is quite variable and IOF area cannot be used to solely predict the presence of whisking, whisking mammals all have large IOF areas. Generally, this pattern holds true regardless of an animal's substrate preferences or activity patterns. Data from fossil mammals and ancestral character state reconstruction and tracing techniques for extant mammals suggest that whisking is not the ancestral state for therian mammals. Instead, whisking appears to have evolved independently as many as seven times across the clades Marsupialia, Afrosoricida, Eulipotyphla, and Rodentia, with Xenarthra the only placental superordinal clade lacking whisking species. However, the term whisking only captures symmetrical and rhythmic movements of the whiskers, rather than all possible whisker movements, and early mammals may still have had moveable whiskers. Anat Rec, 2018. © 2018 American Association for Anatomy.

Recommendations for measuring whisker movements and locomotion in mice with sensory, motor and cognitive deficits.

BACKGROUND: Previous studies have measured whisker movements and locomotion to characterise mouse models of neurodegenerative disease. However, these studies have always been completed in isolation, and do not involve standardized procedures for comparisons across multiple mouse models and background strains. NEW METHOD: We present a standard method for conducting whisker movement and locomotion studies, by carrying out qualitative scoring and quantitative measurement of whisker movements from high-speed video footage of mouse models of Amyotrophic Lateral Sclerosis, Huntington's disease, Parkinson's disease, Alzheimer's disease, Cerebellar Ataxia, Somatosensory Cortex Development and Ischemic stroke. RESULTS: Sex, background strain, source breeder and genotype all affected whisker movements. All mouse models, apart from Parkinson's disease, revealed differences in whisker movements during locomotion. R6/2 CAG250 Huntington's disease mice had the strongest behavioural phenotype. Robo3R3-5-CKO and RIM-DKOSert mouse models have abnormal somatosensory cortex development and revealed significant changes in whisker movements during object exploration. COMPARISON WITH EXISTING METHOD(S): Our results have good agreement with past studies, which indicates the robustness and reliability of measuring whisking. We recommend that differences in whisker movements of mice with motor deficits can be captured in open field arenas, but that mice with impairments to sensory or cognitive functioning should also be filmed investigating objects. Scoring clips qualitatively before tracking will help to structure later analyses. CONCLUSIONS: Studying whisker movements provides a quantitative measure of sensing, motor control and exploration. However, the effect of background strain, sex and age on whisker movements needs to be better understood.