Thermoconforming rays of the star-nosed mole.

The star-nosed mole (Condylura cristata) is renowned for its densely innervated 22 appendage star-like rostrum ('star') specialized for tactile sensation. As a northerly distributed insectivorous mammal exploiting aquatic and terrestrial habitats, these vascularized nasal rays are regularly exposed to cold water and thermally conductive soil, leading us to ask whether the star surface temperature, a proxy for blood flow, conforms to the local ambient temperature to conserve body heat. Alternatively, given the exquisite sensory nature of the star, we posited that the uninsulated rays may be kept warm when foraging to maintain high mechanosensory function. To test these hypotheses, we remotely monitored surface temperatures in wild-caught star-nosed moles. Although the tail acted as a thermal window exhibiting clear vasoconstriction/vasodilation, the star varied passively in surface temperature, with little evidence for thermoregulatory vasomotion. This thermoconforming response may have evolved to minimize conductive heat loss to the water or wet soils when foraging.

Comparative morpho-functional analysis of the humerus and ulna in three Western European moles species of the genus Talpa, including the newly described T. aquitania.

The forelimb is involved in many behaviours including locomotion. Notably, the humero-ulnar articulation, implicated in the elbow joint, is of particular importance for both mobility and stability. Functional constraints, induced in part by environmental plasticity, are thought to drive an important part of the bone shape as bone directly responds and remodels in response to both muscle and external forces. In this context, the study of subterranean moles is of particular interest. These moles occupy a hard and heavy medium in comparison with air or water, requiring a powerful body structure to shear and shift the soil. Their general morphology is therefore adapted to digging and to their subterranean lifestyle. The various morpho-functional patterns, which drive diverse abilities according to the environment, are likely targets of natural selection and it is, therefore, useful to understand the relationships between the bone shape and their function. Here, we quantify, through 3D geometric morphometric methods, the interspecific variability in the morphology of the ulna and humerus of three Talpa species, including the new species Talpa aquitania, to infer their potential consequence in species digging performance. We also quantify shape covariation and morphological integration between the humerus and the ulna to test whether these bones evolve as a uniform functional unit or as more or less independent modules. Our results show that interspecific anatomical differences in the humerus and ulna exist among the three species. Shape changes are mostly located at the level of joints and muscle attachments. As the species tend to live in allopatry and the fossorial lifestyle induces strong ecological constraints, interspecific variations could be explained by the properties of the environment in which they live, such as the compactness of the soil. Our results also show that the humerus and ulna are highly integrated. The covariation between the humerus and ulna in moles is dominated by variation in the attachment areas and particularly of the attachment areas of shoulder muscles concerning the humerus, which affect the mechanical force deployed during locomotion and digging. This study also highlights that in the new species, T. aquitania, variations in anatomical structure (general shape and joints) exist and are related to the locality of collect of the individuals.

Trapped in the morphospace: The relationship between morphological integration and functional performance.

The evolution of complex morphological structures can be characterized by the interplay between different anatomical regions evolving under functional integration in response to shared selective pressures. Using the highly derived humeral morphology of talpid moles as a model, here we test whether functional performance is linked to increased levels of evolutionary integration between humerus subunits and, if so, what the strength is of the relationship. Combining two-dimensional geometric morphometrics, phylogenetic comparative methods, and functional landscape modeling, we demonstrate that the high biomechanical performance of subterranean moles' humeri is coupled with elevated levels of integration, whereas taxa with low-performance values show intermediate or low integration. Theoretical morphs occurring in high-performance areas of the functional landscape are not occupied by any species, and show a marked drop in covariation levels, suggesting the existence of a strong relationship between integration and performance in the evolution of talpid moles' humeri. We argue that the relative temporal invariance of the subterranean environment may have contributed to stabilize humeral morphology, trapping subterranean moles in a narrow region of the landscape and impeding any attempt to reposition on a new ascending slope.

A star-nose-like tactile-olfactory bionic sensing array for robust object recognition in non-visual environments.

Object recognition is among the basic survival skills of human beings and other animals. To date, artificial intelligence (AI) assisted high-performance object recognition is primarily visual-based, empowered by the rapid development of sensing and computational capabilities. Here, we report a tactile-olfactory sensing array, which was inspired by the natural sense-fusion system of star-nose mole, and can permit real-time acquisition of the local topography, stiffness, and odor of a variety of objects without visual input. The tactile-olfactory information is processed by a bioinspired olfactory-tactile associated machine-learning algorithm, essentially mimicking the biological fusion procedures in the neural system of the star-nose mole. Aiming to achieve human identification during rescue missions in challenging environments such as dark or buried scenarios, our tactile-olfactory intelligent sensing system could classify 11 typical objects with an accuracy of 96.9% in a simulated rescue scenario at a fire department test site. The tactile-olfactory bionic sensing system required no visual input and showed superior tolerance to environmental interference, highlighting its great potential for robust object recognition in difficult environments where other methods fall short.

All in the Family - Touch Versus Olfaction in Moles.

Here I review, compare, and contrast the neurobiology and behavior of the common, eastern mole (Scalopus aquaticus) and the star-nosed mole (Condylura cristata). These two species are part of the same family (Talpidae) and have similar body size and general morphology. But they differ in sensory specializations, complexity of neocortical organization, and behavior. The star-nosed mole has an elaborate mechanosensory organ-the star-consisting of 22 epidermal appendages (rays) covered with 25,000 touch domes called Eimer's organs. This densely innervated structure is represented in the neocortex in three different somatosensory maps, each visible in flattened neocortical sections as a series of 11 modules representing the 11 rays from the contralateral body. The 11th ray is greatly magnified in primary somatosensory cortex (S1). Behavioral studies show the star is moved in a saccadic manner and the 11th ray is a high-resolution tactile fovea, allowing star-nosed moles to forage on small prey with unprecedented speed and efficiency. In contrast, common mole noses lack Eimer's organs, their neocortex contains only two cortical maps of the nose, and they cannot localize small prey. Yet common moles have exceptional olfactory abilities, sniffing in stereo to rapidly localize discrete odor sources originating from larger prey. In addition, common moles are shown to track odorant trails laid down by moving prey. These results highlight the surprising abilities of species once thought to be simple, and the usefulness of diverse species in revealing general principles of brain organization and behavior. Anat Rec, 2019. © 2019 American Association for Anatomy.

The variable heartbeat of Japanese moles (Mogera spp.).

This report demonstrates the variable cardiac rhythm in two species of subterranean mole, the large Japanese mole (Mogera wogura) and the lesser Japanese mole (Mogera imaizumii). The phenomenon was revealed using X-ray videos of M. wogura and investigated in detail using electrocardiogram (ECG) traces recorded with implanted electrodes in this species and M. imaizumii. Cessation of heartbeat and extended R-R intervals were observed in the ECGs from both species during short bouts of rest in wakeful specimens of both species under normoxic conditions at room temperature. The mean durations of R-R intervals were 288.8 ± 3.3 ms for M. wogura and 191.9 ± 2.4 ms for M. imaizumii. The cardiac rhythm in both species became more unstable and R-R interval was prolonged by 153.5% ± 17.7 after injection of a sympathetic blocker (propranolol), whereas the application of a parasympathetic blocker (atropine) resulted in increasing stability and a reduced interval between R wave peaks (R-R) 64.2% ± 4.8. ECGs of two related soricomorphs, the fossorial Japanese shrew-mole (Urotrichus talpoides) and surface-dwelling Japanese white-toothed shrew (Crocidura dsinezumi) were also recorded and compared for comparison. The heartbeats of these species were relatively stable compared with those of the subterranean moles. Our results indicated clear differences in the physiological cardiac features between the examined members of the Soricomorpha.

Mole senses.

Many people are familiar with the meandering tunnels of moles, far fewer are familiar with the creatures that made them. Such secrecy is, of course, one of the great benefits of burrowing through the earth where few predators can follow. But it's not the only benefit. Soil contains a smorgasbord of nutritious invertebrate prey - hence all the tunneling. In fact the richness of the soil niche has given rise to a diversity of mole species that could be said to resemble the evolutionary diversification of bats, though on a smaller scale. In both cases, mammals have evolved a suite of unique anatomical traits (coincidentally involving modification of the forelimb) that allows them to exploit a huge resource of invertebrate prey that is largely inaccessible to their competitors. For bats the thin, delicate wings were the key innovation, for moles the forelimbs have undergone a similarly dramatic structural shift, but in the opposite direction - the bones have become short, stout, and powerful to act as shovels.

How moles destroy your lawn: the forelimb kinematics of eastern moles in loose and compact substrates.

The interplay between morphological specialization and kinematic flexibility is important for organisms that move between habitats within different substrates. Burrowing is energetically expensive and requires substantial interaction with soil to dislodge and transport it. True moles (Talpidae) have extraordinary forelimb morphologies and a unique ability to dig in loose as well as compact soils, yet we know little of how moles coordinate their forelimb joint kinematics when digging in soils of different compactness. Using marker-based X-ray Reconstruction of Moving Morphology (XROMM), we tested the hypothesis that moles burrow using different forelimb kinematics in loose and compact substrates. We predicted that moles raise mounds of loose soil by performing powerful compacting strokes mainly with long-axis rotation of the humerus (i.e. pronation/supination), but shear compact soil away by performing scratching strokes involving amplified elbow extension, similar to most scratching diggers. We also predicted that in both types of substrate, moles displace soil rearward like other mammalian diggers. Our results support our hypothesis but not the predictions. Eastern moles (Scalopus aquaticus) move substrates upward using compacting strokes in loose substrates and outward from the body midline using scratching strokes in compact substrates; unlike the digging strokes of most mammalian forelimb diggers, the power-stroke of moles itself does not displace substrates directly rearward. Compacting and scratching strokes involve similar ranges of humeral pronation and retraction at the scapulohumeral (shoulder) joint, yet the movements at the elbow and carpal joints differ. Our results demonstrate that the combination of stereotypic movements of the shoulder joint, where the largest digging muscles are located, and flexibility in the elbow and carpal joints makes moles extremely effective diggers in both loose and compact substrates.

Characteristics of Muscle Fiber-Type Distribution in Moles.

Moles are a strictly fossorial Soricomorpha species and possess a suite of specialized adaptations to subterranean life. However, the contractile function of skeletal muscles in moles remains unclear. We compared muscle fiber-type distribution in two mole species (the large Japanese mole and lesser Japanese mole) with that in four other Soricomorpha species that are semi-fossorial, terrestrial, or semi-aquatic (the Japanese shrew-mole, house shrew, Japanese white-toothed shrew, and Japanese water shrew). For a single species, the fiber-type distribution in up to 38 muscles was assessed using immunohistochemical staining and/or gel electrophoresis. We found that slow and fatigue-resistant Type I fibers were absent in almost all muscles of all species studied. Although, the two methods of determining the fiber type did not give identical results, they both revealed that fast Type IIb fibers were absent in mole muscles. The fiber-type distribution was similar among different anatomical regions in the moles. This study demonstrated that the skeletal muscles of moles have a homogenous fiber-type distribution compared with that in Soricomorpha species that are not strictly fossorial. Mole muscles are composed of Type IIa fibers alone or a combination of Type IIa and relatively fast Type IIx fibers. The homogenous fiber-type distribution in mole muscles may be an adaptation to structurally simple subterranean environments, where there is no need to support body weight with the limbs, or to move at high speeds to pursue prey or to escape from predators. Anat Rec, 302:1010-1023, 2019. © 2018 Wiley Periodicals, Inc.

Regressed but Not Gone: Patterns of Vision Gene Loss and Retention in Subterranean Mammals.

Regressive evolution involves the degradation of formerly useful traits as organisms invade novel ecological niches. In animals, committing to a strict subterranean habit can lead to regression of the eyes, likely due to a limited exposure to light. Several lineages of subterranean mammals show evidence of such degeneration, which can include decreased organization of the retina, malformation of the lens, and subcutaneous positioning of the eye. Advances in DNA sequencing have revealed that this regression co-occurs with a degradation of genomic loci encoding visual functions, including protein-coding genes. Other dim light-adapted vertebrates with normal ocular anatomy, such as nocturnal and aquatic species, also demonstrate evidence of visual gene loss, but the absence of comparative studies has led to the untested assumption that subterranean mammals are special in the degree of this genomic regression. Additionally, previous studies have shown that not all vision genes have been lost in subterranean mammals, but it is unclear whether they are under relaxed selection and will ultimately be lost, are maintained due to pleiotropy or if natural selection is favoring the retention of the eye and certain critical underlying loci. Here I report that vision gene loss in subterranean mammals tends to be more extensive in quantity and differs in distribution from other dim light-adapted mammals, although some committed subterranean mammals demonstrate significant overlap with nocturnal microphthalmic species. In addition, blind subterranean mammals retain functional orthologs of non-pleiotropic visual genes that are evolving at rates consistent with purifying selection. Together, these results suggest that although living underground tends to lead to major losses of visual functions, natural selection is maintaining genes that support the eye, perhaps as an organ for circadian and/or circannual entrainment.

Behavioral pieces of neuroethological puzzles.

In this review, I give a first-person account of surprising insights that have come from the behavioral dimension of neuroethological studies in my laboratory. These studies include the early attempts to understand the function of the nose in star-nosed moles and to explore its representation in the neocortex. This led to the discovery of a somatosensory fovea that parallels the visual fovea of primates in several ways. Subsequent experiments to investigate the assumed superiority of star-nosed moles to their relatives when locating food led to the unexpected discovery of stereo olfaction in common moles. The exceptional olfactory abilities of common moles, in turn, helped to explain an unusual bait-collecting technique called "worm-grunting" in the American southeast. Finally, the predatory behavior of tentacled snakes was best understood not by exploring their nervous system, but rather by considering fish nervous systems. These experiences highlight the difficulty of predicting the abilities of animals that have senses foreign to the investigator, and also the rewards of discovering the unexpected.

Internally coupled ears in living mammals.

It is generally held that the right and left middle ears of mammals are acoustically isolated from each other, such that mammals must rely on neural computation to derive sound localisation cues. There are, however, some unusual species in which the middle ear cavities intercommunicate, in which case each ear might be able to act as a pressure-difference receiver. This could improve sound localisation at lower frequencies. The platypus Ornithorhynchus is apparently unique among mammals in that its tympanic cavities are widely open to the pharynx, a morphology resembling that of some non-mammalian tetrapods. The right and left middle ear cavities of certain talpid and golden moles are connected through air passages within the basicranium; one experimental study on Talpa has shown that the middle ears are indeed acoustically coupled by these means. Having a basisphenoid component to the middle ear cavity walls could be an important prerequisite for the development of this form of interaural communication. Little is known about the hearing abilities of platypus, talpid and golden moles, but their audition may well be limited to relatively low frequencies. If so, these mammals could, in principle, benefit from the sound localisation cues available to them through internally coupled ears. Whether or not they actually do remains to be established experimentally.

Somatosensory organ topography across the star of the star-nosed mole (Condylura cristata).

Quantifying somatosensory receptor distribution in glabrous skin is usually difficult because of the diversity of skin receptor subtypes and their location within the dermis and epidermis. However, the glabrous noses of moles are an exception. In most species of moles, the skin on the nose is covered with domed mechanosensory units known as an Eimer's organs. Eimer's organs contain a stereotyped array of different mechanosensory neurons, meaning that the distribution of mechanosensitive nerve endings can be inferred by visual inspection of the skin surface. Here we detail the distribution of Eimer's organs on the highly derived somatosensory star on the rostrum of the star-nosed mole (Condylura cristata). The star consists of 22 fleshy appendages, or rays, that are covered in Eimer's organs. We find that the density of Eimer's organs increases from proximal to distal locations along the length of the star's rays with a ratio of 1:2.3:3.1 from the surface nearest to the nostril, to the middle part of ray, to the ray tip, respectively. This ratio is comparable to the increase in receptor unit density reported for the human hand, from the palm, to the middle of the digits, to the distal fingertips. We also note that the tactile fovea of the star-nosed mole, located on the medial ventral ray, does not have increased sensory organ density, and we describe these findings in comparison with other sensory fovea.

Reproduction, aging and mortality rate in social subterranean mole voles (Ellobius talpinus Pall.).

Eusocial subterranean rodents of the Bathyergidae family have enormous longevity. The long lifespan of these species is associated with negligible senescence, that is, an absence of the signs of age-related deterioration in physical condition. The question arises as to whether these features are unique to eusocial Bathyergids or typical of other social subterranean rodents as well. In the present study, we analysed data from observations of a social subterranean Microtinae rodent, the northern mole vole (Ellobius talpinus Pall.), which, like mole-rats, has reproductive skew. Among the individuals captured in the wild and maintained in captivity, females that reproduced lived significantly longer than non-breeding females. We did not find any changes in muscle strength with age in any of the demographic groups studied. Faecal glucocorticoid concentrations before death were significantly higher in non-breeding females than in breeding females and males. Increased adrenocortical activity may be one mechanism responsible for the decreased lifespan of non-reproducing individuals of social subterranean rodents. We conclude that the patterns of aging, although different in some respects, are generally common for social subterranean rodents of different taxonomic groups.

Compartmentation of the cerebellar cortex: adaptation to lifestyle in the star-nosed mole Condylura cristata.

The adult mammalian cerebellum is histologically uniform. However, concealed beneath the simple laminar architecture, it is organized rostrocaudally and mediolaterally into complex arrays of transverse zones and parasagittal stripes that is both highly reproducible between individuals and generally conserved across mammals and birds. Beyond this conservation, the general architecture appears to be adapted to the animal's way of life. To test this hypothesis, we have examined cerebellar compartmentation in the talpid star-nosed mole Condylura cristata. The star-nosed mole leads a subterranean life. It is largely blind and instead uses an array of fleshy appendages (the "star") to navigate and locate its prey. The hypothesis suggests that cerebellar architecture would be modified to reduce regions receiving visual input and expand those that receive trigeminal afferents from the star. Zebrin II and phospholipase Cß4 (PLCß4) immunocytochemistry was used to map the zone-and-stripe architecture of the cerebellum of the adult star-nosed mole. The general zone-and-stripe architecture characteristic of all mammals is present in the star-nosed mole. In the vermis, the four typical transverse zones are present, two with alternating zebrin II/PLCß4 stripes, two wholly zebrin II+/PLCß4-. However, the central and nodular zones (prominent visual receiving areas) are proportionally reduced in size and conversely, the trigeminal-receiving areas (the posterior zone of the vermis and crus I/II of the hemispheres) are uncharacteristically large. We therefore conclude that cerebellar architecture is generally conserved across the Mammalia but adapted to the specific lifestyle of the species.

Brain mass and cranial nerve size in shrews and moles.

We investigated the relationship between body size, brain size, and fibers in selected cranial nerves in shrews and moles. Species include tiny masked shrews (S. cinereus) weighing only a few grams and much larger mole species weighing up to 90 grams. It also includes closely related species with very different sensory specializations - such as the star-nosed mole and the common, eastern mole. We found that moles and shrews have tiny optic nerves with fiber counts not correlated with body or brain size. Auditory nerves were similarly small but increased in fiber number with increasing brain and body size. Trigeminal nerve number was by far the largest and also increased with increasing brain and body size. The star-nosed mole was an outlier, with more than twice the number of trigeminal nerve fibers than any other species. Despite this hypertrophied cranial nerve, star-nosed mole brains were not larger than predicted from body size, suggesting that magnification of their somatosensory systems does not result in greater overall CNS size.

The placentation of eulipotyphla-reconstructing a morphotype of the Mammalian placenta.

Placentation determines the developmental status of the neonate, which can be considered as the most vulnerable stage in the mammalian life cycle. In this respect, the different evolutionary and ecological adaptations of marsupial and placental mammals have most likely been associated with the different reproductive strategies of the two therian clades. The morphotypes of marsupial and placental neonates, as well as the placental stem species pattern of Marsupialia, have already been reconstructed. To contribute to a better understanding of the evolution of Placentalia, a histological and ultrastructural investigation of the placenta in three representatives of Eulipotyphla, that is, core insectivores, has been carried out in this study. We studied the Musk shrew (Suncus murinus), the four-toed hedgehog (Atelerix albiventris), and the Iberian mole (Talpa occidentalis). As a result, a eulipotyphlan placental morphotype consisting of a compact and invasive placenta was reconstructed. This supports the widely accepted hypothesis that the stem lineage of Placentalia is characterized by an invasive, either endothelio- or hemochorial placenta. Evolutionary transformations toward a diffuse, noninvasive placenta occurred in the stem lineages of lower primates and cetartiodactyles and were associated with prolonged gestation and the production of few and highly precocial neonates. Compared to the choriovitelline placenta of Marsupialia, the chorioallantoic placenta of Placentalia allows for a more intimate contact and is associated with more advanced neonates.