Innovative problem-solving in a small, wild canid.

Innovation - the ability to solve problems in a novel way - is not only associated with cognitive abilities and relative brain size, but also by noncognitive traits, such as personality and motivation. We used a novel foraging task with three access options to determine how neophobia, exploration, and persistence influence innovation in 12 habituated bat-eared foxes (Otocyon megalotis) in the Kalahari Desert. Bat-eared foxes offer a unique system to understand cognition as they have the smallest relative brain size of measured canids and a specialized, termite-based diet, yet have displayed foraging innovations. Interestingly, most of our individuals solved the task at least once and six individuals solved the task in every trial. Neophobia did not influence success on the first trial, but both exploration and persistence influenced success across all trials. Those individuals that solved the puzzle over multiple trials became faster over time, suggesting that they learned how to open the box more efficiently. We found some variation in the method to open the puzzle box with six individuals solving the puzzle using two methods and one individual using all three methods. This is the first study to show innovation in a novel foraging task in wild bat-eared foxes.

Oxidative stress in response to heat stress in wild caught Namaqua rock mice, Micaelamys namaquensis.

Modelling of anthropogenic induced climate suggests more frequent and severe heatwaves in the future, which are likely to result in the mass die-off of several species of organisms. Oxidative stress induced by severe heat stress has previously been associated with a reduction in animal cognitive performance, depressed reproduction and lower life expectancy. Little is known about the non-lethal consequences of species should they survive extreme heat exposure. We investigated the oxidative stress experienced by the Namaqua rock mouse, a nocturnal rodent, using two experimental heat stress protocols, a 6 hour acute heat stress protocol without access to water and a 3-day heatwave simulation with ad libitum water. Oxidative stress was determined in the liver, kidney and brain using malondialdehyde (MDA) and protein carbonyl (PC) as markers of oxidative damage, and superoxide dismutase (SOD) and total antioxidant capacity (TAC) as markers of antioxidant defence. Incubator heat stress (heat and dehydration stress) was brought about by increasing the body temperatures of animals to 39-40.8 °C for 6 hours. Following incubator heat stress, significantly higher levels of MDA were observed in the liver. Dehydration did not explain the variation in oxidative markers and is likely a combined effect of thermal and dehydration stress. Individual body mass was significantly negatively correlated to kidney SOD and lipid peroxidation. A heatwave was simulated using a temperature cycle that would naturally occur during a heatwave in the species' local habitat, with a maximal ambient temperature of 38 °C. Following the simulated heatwave, SOD activity of the kidney demonstrated significantly lowered activity suggesting oxidative stress. Current heat waves in this species have the potential of causing oxidative stress. Heat and dehydration stress following exacerbated temperatures are likely to incur significant oxidative stress in multiple tissues demonstrating the importance of water availability to allow for rehydration to prevent oxidative stress.

Locomotor activity in field captured crepuscular four-striped field mice, Rhabdomys dilectus and nocturnal Namaqua rock mice, Micaelamys namaquensis during a simulated heat wave.

Activity of animals is influenced by ambient temperature and increasing temperatures brought about by climate change may impose a heat stress risk. Previous studies investigating the effect of heat waves on activity usually measure animals at different, but constant temperatures, however, rarely are they studied under a natural temperature cycle. General activity, behavioural flexibility and frequency of water drinking counts during a normal day, hot day and a simulated heat wave temperature cycle were studied in the crepuscular four-striped field mouse, Rhabdomys dilectus, and the nocturnal Namaqua rock mouse, Micaelamys namaquensis. Both R. dilectus and M. namaquensis showed typical daily locomotor activity under control conditions. During the heat wave, peak activity times changed for R. dilectus, but both species exhibited higher bouts of activity for the heat wave during the day compared to the control, which was accompanied by an increased amount of time spent drinking water. The increased activity during the heat wave is likely due to enhanced water requirements and potentially a form of behavioural thermoregulation as animals may be uncomfortable and try to move to cooler areas. Thus, in the absence of a typical microclimate, access to water may allow rodents to overcome heat stress from extreme temperatures without having to shift their temporal active times.

The role of ambient temperature and light as cues in the control of circadian rhythms of Damaraland mole-rat.

Light is considered the primary entrainer for mammalian biological rhythms, including locomotor activity (LA). However, mammals experience different environmental and light conditions, which include those predominantly devoid of light stimuli, such as those experienced in subterranean environments. In this study, we investigated what environmental cue (light or ambient temperature (Ta)) is the strongest modulator of circadian rhythms, by using LA as a proxy, in mammals that experience a lifestyle devoid of light stimuli. To address this question, this study exposed a subterranean African mole-rat species, the Damaraland mole-rat (Fukomys damarensis), to six light and Ta cycles in different combinations. Contrary to previous literature, when provided with a reliable light cue, Damaraland mole rats exhibited nocturnal, diurnal, or arrhythmic LA patterns under constant Ta. While under constant darkness and a 24-hour Ta cycle mimicking the burrow environment, all mole-rats were most active during the coolest 12-hour period. This finding suggests that in a subterranean environment, which receives no reliable photic cue, the limited heat dissipation and energy constraints during digging activity experienced by Damaraland mole-rats make Ta a reliable and consistent "time-keeping" variable. More so, when providing a reliable light cue (12 light: 12 dark) to Damaraland mole-rats under a 24-hour Ta cycle, this study presents the first evidence that cycles of Ta affect the LA rhythm of a subterranean mammal more strongly than cycles of light and darkness. Once again, Damaraland mole-rats were more active during the coolest 12-hour period regardless of whether this fell during the light or dark phase. However, conclusive differentiation of entrainment to Ta from that of masking was not achieved in this study, and as such, we have recommended future research avenues to do so.

Laterality in the Damaraland Mole-Rat: Insights from a Eusocial Mammal.

Lateralization is the functional control of certain behaviors in the brain being processed by either the left or right hemisphere. Behavioral asymmetries can occur at an individual and population level, although population-level lateralization is less common amongst solitary species, whereas social species can benefit more from aligning and coordinating their activities. We assessed laterality (individual and population) through turning biases in the eusocial Damaraland mole rat, Fukomys damarensis. We considered factors such as breeding status (queen or subordinate), environment (wild-caught or captive), sex (male or female), colony and body mass. All individuals together demonstrated significant left-turning biases, which was also significant at the population level. Wild-caught animals were more strongly lateralized, had a wider spread over a laterality index and lacked the population-level left-turning bias as compared to captive mole rats. Subordinate animals were more lateralized than queens, demonstrating social status differences in turning biases for social mole rats. This emphasizes the importance of animal handling and context when measuring and interpreting behavioral asymmetries.

The Evolution and Ecology of Oxidative and Antioxidant Status: A Comparative Approach in African Mole-Rats.

The naked mole-rat of the family Bathyergidae has been the showpiece for ageing research as they contradict the traditional understanding of the oxidative stress theory of ageing. Some other bathyergids also possess increased lifespans, but there has been a remarkable lack of comparison between species within the family Bathyergidae. This study set out to investigate how plasma oxidative markers (total oxidant status (TOS), total antioxidant capacity (TAC), and the oxidative stress index (OSI)) differ between five species and three subspecies of bathyergids, differing in their maximum lifespan potential (MLSP), resting metabolic rate, aridity index (AI), and sociality. We also investigated how oxidative markers may differ between captive and wild-caught mole-rats. Our results reveal that increased TOS, TAC, and OSI are associated with increased MLSP. This pattern is more prevalent in the social-living species than the solitary-living species. We also found that oxidative variables decreased with an increasing AI and that wild-caught individuals typically have higher antioxidants. We speculate that the correlation between higher oxidative markers and MLSP is due to the hypoxia-tolerance of the mole-rats investigated. Hormesis (the biphasic response to oxidative stress promoting protection) is a likely mechanism behind the increased oxidative markers observed and promotes longevity in some members of the Bathyergidae family.

Defining the link between oxidative stress, behavioural reproductive suppression and heterothermy in the Natal mole-rat (Cryptomys hottentotus natalensis).

Sub-lethal effects, such as oxidative stress, can be linked to various breeding and thermophysiological strategies, which themselves can be linked to seasonal variability in abiotic factors. In this study, we investigated the subterranean, social living Natal mole-rat (Cryptomys hottentotus natalensis), which, unlike other social mole-rat species, implements heterothermy seasonally in an attempt to avoid exercise-induced hyperthermia and relies solely on behavioural reproductive suppression to maintain reproductive skew in colonies. Subsequently, we investigated how oxidative stress varied between season, sex and breeding status in Natal mole-rats. Oxidative markers included total oxidant status (TOS measure of total peroxides present), total antioxidant capacity (TAC), OSI (oxidative stress index) and malondialdehyde (MDA) to measure oxidative stress. Breeding and non-breeding mole-rats of both sexes were captured during the summer (wet season) and winter (dry season). Seasonal environmental variables (air temperature, soil temperature and soil moisture) had a significant effect on TOS, OSI and MDA, where season affected each sex differently. Unlike other social mole-rat species that use both physiological and behavioural means of reproductive suppression, no oxidative costs to reproduction were present in the Natal mole-rats. Males had significantly higher MDA than females, which was most apparent in summer (wet season). We conclude that the significant oxidative damage in males is a consequence of exercise-induced oxidative stress, exacerbated by increased burrow humidities and poorer heat dissipation abilities as a function of body mass. This study highlights the importance of both breeding and thermophysiological strategies in affecting oxidative stress.

Tissue Oxidative Ecology along an Aridity Gradient in a Mammalian Subterranean Species.

Climate change has caused aridification which can alter habitat vegetation, soil and precipitation profiles potentially affecting resident species. Vegetation and soil profiles are important for subterranean mole-rats as increasing aridity causes soils to become harder and geophytes less evenly distributed, and the inter-geophyte distance increases. Mole-rats obtain all water and dietary requirements from geophytes, and thus digging in harder soils may amplify stressors (hyperthermia, dehydration- or exercise-induced damage). This study assessed the oxidative status of the wild common mole-rat along an aridity gradient (arid, semi-arid and mesic). Kidney and liver oxidative markers, including total oxidant status (TOS), total antioxidant capacity (TAC), oxidative stress index (OSI), malondialdehyde (MDA) and superoxide dismutase (SOD) were measured. Liver oxidative status did not demonstrate any significance with the degree of the aridity gradient. Aridity affected the TAC and OSI of the kidney, with individuals in the most arid habitats possessing the highest TAC. The evolution of increased group size to promote survival in African mole-rats in arid habitats may have resulted in the additional benefit of reduced oxidative stress in the kidneys. The SOD activity of the kidneys was higher than that of the liver with lower oxidative damage, suggesting this species pre-emptively protects its kidneys as these are important for water balance and retention.

Laterality in the Cape mole-rat, Georychus capensis.

Behavioural lateralization, the differential use one side of the body, and/or the bilateral use of sensory organs or limbs, is common in many vertebrates. One way in which behavioural lateralization can be detected in animals is through turning biases, which is an inherent preference to either turn left or right. Mole-rats are a unique group of mammals that demonstrate a wide range of social organizations ranging from solitary to eusociality. Behavioural asymmetry has not previously been investigated in mole-rats. In this study, captive and wild solitary Cape-mole rats (Georychus capensis) were investigated for individual (relative laterality (LR)) and population-level (absolute laterality (LA)) laterality. Mole-rats in the captive group were in the laboratory for at least one year, whereas the wild group were captured and experimented on within 2 weeks of capture. Animals were placed in a Y-maze facing away from the centre of the maze, and the turn towards the centre of the maze was evaluated to determine individual turning biases. Lateralized individual turning biases were more apparent in wild (7/9), compared to captive (3/10) individuals. Both captive and wild populations demonstrated a left bias, which was higher in wild animals, but not significantly so. Cape mole-rats are extremely xenophobic and aggressive, and this aggressive behaviour may underlie the turning biases in these animals, as aggression is primarily a right hemisphere dominant process. The reduced lateralization observed in captive animals may be due to a reduced need for these behaviours as a result of different environments in captivity.

Heat and dehydration induced oxidative damage and antioxidant defenses following incubator heat stress and a simulated heat wave in wild caught four-striped field mice Rhabdomys dilectus.

Heat waves are known for their disastrous mass die-off effects due to dehydration and cell damage, but little is known about the non-lethal consequences of surviving severe heat exposure. Severe heat exposure can cause oxidative stress which can have negative consequences on animal cognition, reproduction and life expectancy. We investigated the current oxidative stress experienced by a mesic mouse species, the four striped field mouse, Rhabdomys dilectus through a heat wave simulation with ad lib water and a more severe temperature exposure with minimal water. Wild four striped field mice were caught between 2017 and 2019. We predicted that wild four striped field mice in the heat wave simulation would show less susceptibility to oxidative stress as compared to a more severe heat stress which is likely to occur in the future. Oxidative stress was determined in the liver, kidney and brain using malondialdehyde (MDA) and protein carbonyl (PC) as markers for oxidative damage, and superoxide dismutase (SOD) and total antioxidant capacity (TAC) as markers of antioxidant defense. Incubator heat stress was brought about by increasing the body temperatures of animals to 39-40.8°C for 6 hours. A heat wave (one hot day, followed by a 3-day heatwave) was simulated by using temperature cycle that wild four striped field mice would experience in their local habitat (determined through weather station data using temperature and humidity), with maximal ambient temperature of 39°C. The liver and kidney demonstrated no changes in the simulated heat wave, but the liver had significantly higher SOD activity and the kidney had significantly higher lipid peroxidation in the incubator experiment. Dehydration significantly contributed to the increase of these markers, as is evident from the decrease in body mass after the experiment. The brain only showed significantly higher lipid peroxidation following the simulated heat wave with no significant changes following the incubator experiment. The significant increase in lipid peroxidation was not correlated to body mass after the experiment. The magnitude and duration of heat stress, in conjunction with dehydration, played a critical role in the oxidative stress experienced by each tissue, with the results demonstrating the importance of measuring multiple tissues to determine the physiological state of an animal. Current heat waves in this species have the potential of causing oxidative stress in the brain with future heat waves to possibly stress the kidney and liver depending on the hydration state of animals.

Experimental sources of variation in avian energetics: estimated basal metabolic rate decreases with successive measurements.

Basal metabolic rate (BMR) is one of the most widely used metabolic variables in endotherm ecological and evolutionary physiology. Surprisingly few studies have investigated how BMR is influenced by experimental and analytical variables over and above the standardized conditions required for minimum normothermic resting metabolism. We tested whether avian BMR is affected by habituation to the conditions experienced during laboratory gas exchange measurements by measuring BMR five times in succession in budgerigars (Melopsittacus undulatus) housed under constant temperature and photoperiod. Both the magnitude and the variability of BMR decreased significantly with repeated measurements, from 0.410 ± 0.092 W (n = 9) during the first measurement to 0.285 ± 0.042 W (n = 9) during the fifth measurement. Thus, estimated BMR decreased by ∼30% within individuals solely on account of the number of times they had previously experienced the experimental conditions. The most likely explanation for these results is an attenuation with repeated exposure of the acute stress response induced by birds being handled and placed in respirometry chambers. Our data suggest that habituation to experimental conditions is potentially an important determinant of observed BMR, and this source of variation needs to be taken into account in future studies of metabolic variation among individuals, populations, and species.

Lip repositioning with reversible trial for the management of excessive gingival display: a case series.

Lip repositioning surgery is a largely unknown and underutilized treatment modality for excessive gingival display. It involves precise resection of maxillary mucosal tissues with reattachment of the lip in a more coronal position. This limits lip elevation on smiling and increases lip fullness. While this is an elective treatment, no reported cases have yet offered patients the ability to preview the outcome in a reversible manner. This case series presents seven patients who were successfully managed with trial, and then definitive, lip repositioning.