A GPS assisted translocation experiment to study the homing behavior of red deer.

Many animals return to their home areas (i.e., 'homing') after translocation to sites further away. Such translocations have traditionally been used in behavioral ecology to understand the orientation and migration behavior of animals. The movement itself can then be followed by marking and recapturing animals or by tracking, for example, using GPS systems. Most detailed studies investigating this behavior have been conducted in smaller vertebrates (e.g., birds, amphibians, and mice), whereas information on larger mammals, such as red deer, is sparse. We conducted GPS-assisted translocation experiments with red deer at two sites in the Czech Republic. Individuals were translocated over a distance of approximately 11 km and their home journey was tracked. Circular statistics were used to test for significant homeward orientation at distances of 100, 500, 1000, and 5000 m from the release site. In addition, we applied Lavielle trajectory segmentation to identify the different phases of homing behavior. Thirty-one out of 35 translocations resulted in successful homing, with a median time of 4.75 days (range 1.23-100 days). Animals were significantly oriented towards home immediately after release and again when they came closer to home; however, they did not show a significant orientation at the distances in between. We were able to identify three homing phases, an initial 'exploratory phase', followed by a 'homing phase' which sometimes was again followed by an 'arrival phase'. The 'homing phase' was characterized by the straightest paths and fastest movements. However, the variation between translocation events was considerable. We showed good homing abilities of red deer after translocation. Our results demonstrate the feasibility of conducting experiments with environmental manipulations (e.g., to impede the use of sensory cues) close to the release site. The homing behavior of red deer is comparable to that of other species, and might represent general homing behavior patterns in animals. Follow-up studies should further dissect and investigate the drivers of the individual variations observed and try to identify the sensory cues used during homing.

Investigating the impact of weak geomagnetic fluctuations on pigeon races.

The existence of avian magnetic orientation has been proved by many experimental studies, however, evidence for the use of magnetic cues by homing pigeons remains controversial. To investigate magnetic orientation by homing pigeons, we analyzed the results of pigeon races relative to weak fluctuations in the geomagnetic field, assuming that such disturbances could impact navigational efficiency if based on magnetoreception. Whereas most of the previous studies recorded and analyzed vanishing bearing of individually released pigeons, we evaluated relative duration of the homeward flight (homing speed, as a proxy of navigational efficiency) and its dependence on specific geomagnetic indices in racing pigeons released collectively. Our analysis of orientation efficiency of about 289 pigeon races over 15 years suggested slight negative correlations between geomagnetic fluctuations and homing time. Although the interpretation of this finding is manifold and not clear, it suggests that natural magnetic variations or disturbances can affect the homing orientation performance of pigeons. We suggest that studying pigeon races may have a heuristic potential and since these races are regularly and frequently organized in many countries all over the globe, examining homing performance relative to a suite of environmental variables may be useful for exploring hypotheses about pigeon navigation.

Observation of rescue behaviour in wild boar (Sus scrofa).

Here, we provide unique photo documentation and observational evidence of rescue behaviour described for the first time in wild boar. Rescue behaviour represents an extreme form of prosocial behaviour that has so far only been demonstrated in a few species. It refers to a situation when one individual acts to help another individual that finds itself in a dangerous or stressful situation and it is considered by some authors as a complex form of empathy. We documented a case in which an adult female wild boar manipulated wooden logs securing the door mechanism of a cage trap and released two entrapped young wild boars. The whole rescue was fast and particular behaviours were complex and precisely targeted, suggesting profound prosocial tendencies and exceptional problem-solving capacities in wild boar. The rescue behaviour might have been motivated by empathy because the rescuer female exhibited piloerection, a sign of distress, indicating an empathetic emotional state matching or understanding the victims. We discuss this rescue behaviour in the light of possible underlying motivators, including empathy, learning and social facilitation.

Ear morphology in two root-rat species (genus Tachyoryctes) differing in the degree of fossoriality.

It is supposed that the subterranean lifestyle in mammals is reflected in ear morphology and tuning of hearing to low frequencies. We studied two root-rat species to see if their ear morphology reflects the difference in the amount of their surface activity. Whereas the more subterranean Tachyoryctes splendens possesses shorter pinnae as expected, it has smaller bullae compared to the more epigeic Tachyoryctes macrocephalus. The ratio between the eardrum and the stapedial footplate area and the ratio between the mallear and the incudal lever were lower in T. splendens (19.3 ± 0.3 and 1.9 ± 0.0, respectively) than in T. macrocephalus (21.8 ± 0.6 and 2.1 ± 0.1), probably reflecting the latter's higher surface activity. The cochlea in both species has 3.5 coils, yet the basilar membrane is longer in the smaller T. splendens (13.0 ± 0.5 versus 11.4 ± 0.7 mm), which indicates its wider hearing range and/or higher sensitivity (to some frequencies). In both root-rat species, the highest density of outer hair cells (OHC) was in the apical part of the cochlea, while the highest density of inner hair cells (IHC) was in its middle part. This OHC density pattern corresponds with good low-frequency hearing, whereas the IHC pattern suggests sensitivity to higher frequencies.

Increased longevity due to sexual activity in mole-rats is associated with transcriptional changes in the HPA stress axis.

Sexual activity and/or reproduction are associated with a doubling of life expectancy in the long-lived rodent genus Fukomys. To investigate the molecular mechanisms underlying this phenomenon, we analyzed 636 RNA-seq samples across 15 tissues. This analysis suggests that changes in the regulation of the hypothalamic-pituitary-adrenal stress axis play a key role regarding the extended life expectancy of reproductive vs. non-reproductive mole-rats. This is substantiated by a corpus of independent evidence. In accordance with previous studies, the up-regulation of the proteasome and so-called 'anti-aging molecules', for example, dehydroepiandrosterone, is linked with enhanced lifespan. On the other hand, several of our results are not consistent with knowledge about aging of short-lived model organisms. For example, we found the up-regulation of the insulin-like growth factor 1/growth hormone axis and several other anabolic processes to be compatible with a considerable lifespan prolongation. These contradictions question the extent to which findings from short-lived species can be transferred to longer-lived ones.

Turning preference in dogs: North attracts while south repels.

It was shown earlier that dogs, when selecting between two dishes with snacks placed in front of them, left and right, prefer to turn either clockwise or counterclockwise or randomly in either direction. This preference (or non-preference) is individually consistent in all trials but it is biased in favor of north if they choose between dishes positioned north and east or north and west, a phenomenon denoted as "pull of the north". Here, we replicated these experiments indoors, in magnetic coils, under natural magnetic field and under magnetic field shifted 90° clockwise. We demonstrate that "pull of the north" was present also in an environment without any outdoor cues and that the magnetic (and not topographic) north exerted the effect. The detailed analysis shows that the phenomenon involves also "repulsion of the south". The clockwise turning preference in the right-preferring dogs is more pronounced in the S-W combination, while the counterclockwise turning preference in the left-preferring dogs is pronounced in the S-E combination. In this way, south-placed dishes are less frequently chosen than would be expected, while the north-placed dishes are apparently more preferred. Turning preference did not correlate with the motoric paw laterality (Kong test). Given that the choice of a dish is visually guided, we postulate that the turning preference was determined by the dominant eye, so that a dominant right eye resulted in clockwise, and a dominant left eye in counterclockwise turning. Assuming further that magnetoreception in canines is based on the radical-pair mechanism, a "conflict of interests" may be expected, if the dominant eye guides turning away from north, yet the contralateral eye "sees the north", which generally acts attractive, provoking body alignment along the north-south axis.

Surprisingly long survival of premature conclusions about naked mole-rat biology.

Naked mole-rats express many unusual traits for such a small rodent. Their morphology, social behaviour, physiology, and ageing have been well studied over the past half-century. Many early findings and speculations about this subterranean species persist in the literature, although some have been repeatedly questioned or refuted. While the popularity of this species as a natural-history curiosity, and oversimplified story-telling in science journalism, might have fuelled the perpetuation of such misconceptions, an accurate understanding of their biology is especially important for this new biomedical model organism. We review 28 of these persistent myths about naked mole-rat sensory abilities, ecophysiology, social behaviour, development and ageing, and where possible we explain how these misunderstandings came about.

Wolf Howling and Emergency Sirens: A Hypothesis of Natural and Technical Convergence of Aposematic Signals.

Acoustic signals serving intraspecific communication by predators are perceived by potential prey as warning signals. We analysed the acoustic characteristics of howling of wolves and found a striking similarity to the warning sounds of technical sirens. We hypothesize that the effectivity of sirens as warning signals has been enhanced by natural sensory predisposition of humans to get alerted by howling of wolves, with which they have a long history of coexistence. Psychoacoustic similarity of both stimuli seems to be supported by the fact that wolves and dogs perceive the sound of technical sirens as a relevant releasing supernormal stimulus and reply to it with howling. Inspiration by naturally occurring acoustic aposematic signals might become an interesting example of biomimetics in designing new warning sound systems.

Low frequencies in the display vocalization of the Western Capercaillie (Tetrao urogallus).

Only a few bird species are known to produce low-frequency vocalizations. We analyzed the display vocalizations of Western Capercaillie males kept in breeding centers and identified harmonically structured signals with a fundamental frequency of 28.7 ± 1.2 Hz (25.6-31.6 Hz). These low-frequency components temporally overlap with the Whetting phase (96% of its duration) and they significantly contribute to the distinct vocal expression between individuals. The resulting model of discrimination analysis classified 67.6% vocalizations (63%, cross-validated result) correctly to the specific individual in comparison to the probability by chance of 12.5%. We discuss a possible function of low-frequency components that remains unclear. The occurrence of such low frequencies is surprising as this grouse is substantially smaller than cassowaries (Southern cassowary Casuarius casuarius and Dwarf cassowary Casuarius bennetti) , the species that produces similarly low frequencies. Because these low frequency components temporarily overlap with the Whetting phase, they are hardly audible from a distance larger than several meters.

Magnetic alignment enhances homing efficiency of hunting dogs.

Despite anecdotal reports of the astonishing homing abilities in dogs, their homing strategies are not fully understood. We equipped 27 hunting dogs with GPS collars and action cams, let them freely roam in forested areas, and analyzed components of homing in over 600 trials. When returning to the owner (homewards), dogs either followed their outbound track ('tracking') or used a novel route ('scouting'). The inbound track during scouting started mostly with a short (about 20 m) run along the north-south geomagnetic axis, irrespective of the actual direction homewards. Performing such a 'compass run' significantly increased homing efficiency. We propose that this run is instrumental for bringing the mental map into register with the magnetic compass and to establish the heading of the animal.

Functional histology of the skin in the subterranean African giant mole-rat: thermal windows are determined solely by pelage characteristics.

Excavation of burrows is an extremely physically demanding activity producing a large amount of metabolic heat. Dissipation of its surplus is crucial to avoid the risk of overheating, but in subterranean mammals it is complicated due to the absence of notable body extremities and high humidity in their burrows. IR-thermography in a previous study on two species of African mole-rats revealed that body heat was dissipated mainly through the ventral body part, which is notably less furred. Here, we analyzed the dorsal and ventral skin morphology, to test if dermal characteristics could contribute to higher heat dissipation through the ventral body part. The thickness of the epidermis and dermis and the presence, extent and connectivity of fat tissue in the dermis were examined using routine histological methods, while vascular density was evaluated using fluorescent dye and confocal microscopy in the giant mole-rat Fukomys mechowii. As in other hitherto studied subterranean mammals, no subcutaneous adipose tissue was found. All examined skin characteristics were very similar for both dorsal and ventral regions: relative content of adipose tissue in the dermis (14.4 ± 3.7% dorsally and 11.0 ± 4.0% ventrally), connectivity of dermal fat (98.5 ± 2.8% and 95.5 ± 6.8%), vascular density (26.5 ± 3.3% and 22.7 ± 2.3%). Absence of large differences in measured characteristics between particular body regions indicates that the thermal windows are determined mainly by the pelage characteristics.

Author Correction: Cryptochrome 1 in Retinal Cone Photoreceptors Suggests a Novel Functional Role in Mammals.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Functional anatomy of the middle and inner ears of the red fox, in comparison to domestic dogs and cats.

Anatomical middle and inner ear parameters are often used to predict hearing sensitivities of mammalian species. Given that ear morphology is substantially affected both by phylogeny and body size, it is interesting to consider whether the relatively small anatomical differences expected in related species of similar size have a noticeable impact on hearing. We present a detailed anatomical description of the middle and inner ears of the red fox Vulpes vulpes, a widespread, wild carnivore for which a behavioural audiogram is available. We compare fox ears to those of the well-studied and similarly sized domestic dog and cat, taking data for dogs and cats from the literature as well as providing new measurements of basilar membrane (BM) length and hair cell numbers and densities in these animals. Our results show that the middle ear of the red fox is very similar to that of dogs. The most obvious difference from that of the cat is the lack of a fully formed bony septum in the bulla tympanica of the fox. The cochlear structures of the fox, however, are very like those of the cat, whereas dogs have a broader BM in the basal cochlea. We further report that the mass of the middle ear ossicles and the bulla volume increase with age in foxes. Overall, the ear structures of foxes, dogs and cats are anatomically very similar, and their behavioural audiograms overlap. However, the results of several published models and correlations that use middle and inner ear measurements to predict aspects of hearing were not always found to match well with audiogram data, especially when it came to the sharper tuning in the fox audiogram. This highlights that, although there is evidently a broad correspondence between structure and function, it is not always possible to draw direct links when considering more subtle differences between related species.

Comment on 'Naked mole-rat mortality rates defy Gompertzian laws by not increasing with age'.

Ruby et al. recently analyzed historical lifespan data on more than 3200 naked mole-rats, collected over a total observation period of about 38 years (Ruby et al., 2018). They report that mortality hazards do not seem to increase across the full range of their so-far-observed lifespan, and conclude that this defiance of Gompertz's law 'uniquely identifies the naked mole-rat as a non-aging mammal'. Here, we explain why we believe this conclusion is premature.

Vocal recognition of a nest-predator in black grouse.

Corvids count among the important predators of bird nests. They are vocal animals and one can expect that birds threatened by their predation, such as black grouse, are sensitive to and recognize their calls. Within the framework of field studies, we noticed that adult black grouse were alerted by raven calls during periods outside the breeding season. Since black grouse are large, extremely precocial birds, this reaction can hardly be explained by sensitization specifically to the threat of nest predation by ravens. This surprising observation prompted us to study the phenomenon more systematically. According to our knowledge, the response of birds to corvid vocalization has been studied in altricial birds only. We tested whether the black grouse distinguishes and responds specifically to playback calls of the common raven. Black grouse recognized raven calls and were alerted, displaying typical neck stretching, followed by head scanning, and eventual escape. Surprisingly, males tended to react faster and exhibited a longer duration of vigilance behavior compared to females. Although raven calls are recognized by adult black grouse out of the nesting period, they are not directly endangered by the raven. We speculate that the responsiveness of adult grouse to raven calls might be explained as a learned response in juveniles from nesting hens that is then preserved in adults, or by a known association between the raven and the red fox. In that case, calls of the raven would be rather interpreted as a warning signal of probable proximity of the red fox.

Brain atlas of the African mole-rat Fukomys anselli.

African mole-rats are subterranean rodents that spend their whole life in underground burrow systems. They show a range of morphological and physiological adaptations to their ecotope, for instance severely reduced eyes and specialized somatosensory, olfactory, and auditory systems. These adaptations are also reflected in the accessory sensory pathways in the brain that process the input coming from the sensory organs. So far, a brain atlas was available only for the naked mole-rat (Heterocephalus glaber). The Ansell's mole-rat (Fukomys anselli) has been the subject of many investigations in various disciplines (ethology, sensory physiology, and anatomy) including magnetic orientation. It is therefore surprising that an atlas of the brain of this species was not available so far. Here, we present a comprehensive atlas of the Ansell's mole-rat brain based on Nissl and Klüver-Barrera stained sections. We identify and label 375 brain regions and discuss selected differences from the brain of the closely related naked mole-rat as well as from epigeic mammals (rat), with a particular focus on the auditory brainstem. This atlas can serve as a reference for future neuroanatomical investigations of subterranean mammals.

Dogs can be trained to find a bar magnet.

Magnetoreception, the ability to sense the Earth's magnetic field (MF), is a widespread phenomenon in the animal kingdom. In 1966, the first report on a magnetosensitive vertebrate, the European robin (Erithacus rubecula), was published. After that, numerous further species of different taxa have been identified to be magnetosensitive as well. Recently, it has been demonstrated that domestic dogs (Canis lupus familiaris) prefer to align their body axis along the North-South axis during territorial marking under calm MF conditions and that they abandon this preference when the Earth's MF is unstable. In a further study conducting a directional two-choice-test, dogs showed a spontaneous preference for the northern direction. Being designated as putatively magnetosensitive and being also known as trainable for diverse choice and search tests, dogs seem to be suitable model animals for a direct test of magnetoreception: learning to find a magnet. Using operant conditioning dogs were trained to identify the MF of a bar magnet in a three-alternative forced-choice experiment. We excluded visual cues and used control trials with food treats to test for the role of olfaction in finding the magnet. While 13 out of 16 dogs detected the magnet significantly above chance level (53-73% success rate), none of the dogs managed to do so in finding the food treat (23-40% success rate). In a replication of the experiment under strictly blinded conditions five out of six dogs detected the magnet above chance level (53-63% success rate). These experiments support the existence of a magnetic sense in domestic dogs. Whether the sense enables dogs to perceive MFs as weak as the Earth's MF, if they use it for orientation, and by which mechanism the fields are perceived remain open questions.

Do subterranean mammals use the Earth's magnetic field as a heading indicator to dig straight tunnels?

Subterranean rodents are able to dig long straight tunnels. Keeping the course of such "runways" is important in the context of optimal foraging strategies and natal or mating dispersal. These tunnels are built in the course of a long time, and in social species, by several animals. Although the ability to keep the course of digging has already been described in the 1950s, its proximate mechanism could still not be satisfactorily explained. Here, we analyzed the directional orientation of 68 burrow systems in five subterranean rodent species (Fukomys anselli, F. mechowii, Heliophobius argenteocinereus, Spalax galili, and Ctenomys talarum) on the base of detailed maps of burrow systems charted within the framework of other studies and provided to us. The directional orientation of the vast majority of all evaluated burrow systems on the individual level (94%) showed a significant deviation from a random distribution. The second order statistics (averaging mean vectors of all the studied burrow systems of a respective species) revealed significant deviations from random distribution with a prevalence of north-south (H. argenteocinereus), NNW-SSE (C. talarum), and NE-SW (Fukomys mole-rats) oriented tunnels. Burrow systems of S. galili were randomly oriented. We suggest that the Earth's magnetic field acts as a common heading indicator, facilitating to keep the course of digging. This study provides a field test and further evidence for magnetoreception and its biological meaning in subterranean mammals. Furthermore, it lays the foundation for future field experiments.

Sociality does not drive the evolution of large brains in eusocial African mole-rats.

The social brain hypothesis (SBH) posits that the demands imposed on individuals by living in cohesive social groups exert a selection pressure favouring the evolution of large brains and complex cognitive abilities. Using volumetry and the isotropic fractionator to determine the size of and numbers of neurons in specific brain regions, here we test this hypothesis in African mole-rats (Bathyergidae). These subterranean rodents exhibit a broad spectrum of social complexity, ranging from strictly solitary through to eusocial cooperative breeders, but feature similar ecologies and life history traits. We found no positive association between sociality and neuroanatomical correlates of information-processing capacity. Solitary species are larger, tend to have greater absolute brain size and have more neurons in the forebrain than social species. The neocortex ratio and neuronal counts correlate negatively with social group size. These results are clearly inconsistent with the SBH and show that the challenges coupled with sociality in this group of rodents do not require brain enlargement or fundamental reorganization. These findings suggest that group living or pair bonding per se does not select strongly for brain enlargement unless coupled with Machiavellian interactions affecting individual fitness.

Attracted by a magnet: Exploration behaviour of rodents in the presence of magnetic objects.

Magnetosensitivity is widespread among animals with rodents being the most intensively studied mammalian group. The available behavioural assays for magnetoreception are time-consuming, which impedes screens for treatment effects that could characterize the enigmatic magnetoreceptors. Here, we present a fast and simple approach to test if an animal responds to magnetic stimuli: the magnetic object assay (MOA). The MOA focuses on investigating an animal's spontaneous exploration behaviour in the presence of a bar magnet compared to a demagnetised control. We present consistently longer exploration of the magnet in three different rodent species: Ansell's mole-rat (Fukomys anselli), C57BL/6J laboratory mouse, and naked mole-rat (Heterocephalus glaber). For the naked mole-rat this is the first report that this species reacts on magnetic stimuli. We conclude that the MOA holds the potential to screen if an animal responds to magnetic stimuli, indicating the possession of a magnetic sense.