Tolerant mothers: aggression does not explain solitary living in the bush Karoo rat.

Many mammal species are thought to adopt solitary living owing to mothers becoming intolerant of adult offspring and the occurrence of social intolerance between adults. However, field studies on how solitary mammals interact are rare. Here we show that solitary living can occur without social intolerance. Over 3 years, we recorded interactions between free-living bush Karoo rats (Otomys unisulcatus) and conducted dyadic encounter experiments between kin and non-kin female neighbours, both in a neutral test arena and in field intruder experiments. Social interactions were rare (230/2062 observations), and they were aggressive in only 34% of cases. In dyadic encounters, mothers interacted amicably with young offspring. Aggression between mothers and offspring was almost absent. This mother-offspring relationship remained amicable even after adult offspring had dispersed. Aggression between neighbouring adult females was low in neutral arena tests, independent of kinship and season. However, in the field, females reacted more aggressively towards non-kin than kin intruders, especially during the breeding season. Tolerance between mothers and adult offspring indicates that aggression is not the mechanism leading to dispersal and solitary living. We found a solitary social system characterized by social tolerance, suggesting that dispersal and lack of social attraction rather than aggression can lead to solitary living.

Cognitive flexibility in urban yellow mongooses, Cynictis penicillata.

Cognitive flexibility enables animals to alter their behaviour and respond appropriately to environmental changes. Such flexibility is important in urban settings where environmental changes occur rapidly and continually. We studied whether free-living, urban-dwelling yellow mongooses, Cynictis penicillata, in South Africa, are cognitively flexible in reversal learning and attention task experiments (n = 10). Reversal learning was conducted using two puzzle boxes that were distinct visually and spatially, each containing a preferred or non-preferred food type. Once mongooses learned which box contained the preferred food type, the food types were reversed. The mongooses successfully unlearned their previously learned response in favour of learning a new response, possibly through a win-stay, lose-shift strategy. Attention task experiments were conducted using one puzzle box surrounded by zero, one, two or three objects, introducing various levels of distraction while solving the task. The mongooses were distracted by two and three distractions but were able to solve the task despite the distractions by splitting their attention between the puzzle box task and remaining vigilant. However, those exposed to human residents more often were more vigilant. We provide the first evidence of cognitive flexibility in urban yellow mongooses, which enables them to modify their behaviour to urban environments.

Cognitive performance is linked to survival in free-living African striped mice.

Cognition is shaped by evolution and is predicted to increase fitness. However, the link between cognition and fitness in free-living animals is unresolved. We studied the correlates of cognition and survival in a free-living rodent inhabiting an arid environment. We tested 143 striped mice (Rhabdomys pumilio) using a battery of cognitive tests, including: (i) an attention task, (ii) two problem-solving tasks, (iii) a learning and reversal learning task, and (iv) an inhibitory control task. We related cognitive performance with days of survival. Better problem-solving and inhibitory control performance were significant correlates of survival. Surviving males showed greater reversal learning which may be related to sex-specific behavioural and life-history characteristics. Specific cognitive traits and not a composite measure of general intelligence underpins fitness in this free-living rodent population, enhancing our understanding of the evolution of cognition in non-human animals.

Seasonal changes in problem-solving in wild African striped mice.

Innovative problem-solving ability is a predictor of whether animals can successfully cope with environmental changes. These environmental changes can test the limits of animals, for example when energy availability decreases seasonally and, hence, problem-solving performance decreases because less energy is available for cognitive processes. Here, we investigated: (1) how problem-solving performance changed between seasons that differed significantly in food availability; (2) whether these changes were related to environmentally induced physiological changes in blood glucose and ketone levels, indicators of energy availability; and (3) whether individual variation in problem-solving was related to sex differences. We studied 99 free-ranging African striped mice, Rhabdomys pumilio, in the Succulent Karoo, South Africa, 55 during the hot dry summer with low food availability and 44 during the cold wet winter with higher food availability. We measured their problem-solving abilities using a food extraction task and found no seasonal differences in problem-solving success. However, mice solved the problem faster in summer versus winter. In summer, food availability was reduced and blood ketones increased but there was no seasonal difference in blood glucose levels. There were no correlation between problem-solving performance and blood glucose or ketone levels. Overall, more males solved the task than females. It appears that in striped mice cognitive functions can be maintained under harsh environmental conditions.

The Development of Anxiety and Exploration in Two Species of the African Striped Mouse Rhabdomys.

Genes and the environment interact to produce complex, environmentally relevant behaviors. We tested whether the behavior of two sister species of striped mice originating from different habitats (semi-arid Rhabdomys pumilio and grassland R. bechuanae) are modulated by the early social rearing environment. We cross-fostered pups between the species, and at adulthood tested their exploratory behavior and anxiety in open field and novel object tests, and a plus maze. We expected that the early social rearing environment would alter the phenotype of both species. Regardless of treatment, R. bechuanae were more exploratory and slightly less anxious than R. pumilio. However, fostered individuals of both species showed no changes in exploratory and anxiety responses. Thus there may be a genetic influence on behavioral development, or the early rearing environments of R. pumilio and R. bechuanae are not sufficiently different to alter behavior.

Do alternative reproductive tactics predict problem-solving performance in African striped mice?

In changing environments, animals face unexpected problems to solve. Not all individuals in a population are equally able to solve new problems. It still remains unclear what factors (e.g. age and body condition) influence the propensity of problem solving. We investigated variation in problem-solving performance among males following alternative reproductive tactics (ARTs). We studied a free-ranging population of the African striped mouse (Rhabdomys pumilio). Adult male striped mice can employ 3 ARTs: (1) dominant group-living breeders, (2) philopatric living in their natal group, and (3) solitary-living roamers. ARTs in male striped mice reflect differences in competitiveness, sociality and physiology which could influence their problem-solving performance. We tested a total of 48 males in 2 years with two tasks: a string-pulling task to reach food and a door-opening task to reach the nest. Since male striped mice differ in personality traits independent of ARTs, we also measured activity, boldness and exploration. In addition, we assessed the association of body condition and age with problem solving. Problem solving was related the interaction of age and ARTs. The younger philopatrics had better performance in a food-extraction task whereas the older breeders were faster at solving the door-opening task. Individual differences in traits related to personality were significant correlates of problem-solving performance: pro-active mice (i.e. more active and explorative and bolder) performed better in both tasks. Finally, problem-solving performance was not consistent between the two tasks. Our study provides evidence of correlates of ARTs, age and personality on problem-solving abilities.

Sons benefit from paternal care in African striped mice.

Mammalian paternal care is rare and is often linked to enhanced fitness under particular ecological conditions. The proximate consequences of paternal care on offspring are lacking, however. Here, we tested whether levels of paternal care predict the behavioural, cognitive and physiological development of sons in the naturally paternal African striped mouse (Rhabdomys pumilio). We focused on sons raised in two treatments: biparental (both parents) or uniparental (mother alone) families. We recorded levels of interactions between pups with both parents, and later assessed the behaviour, cognition and physiology of sons at three developmental stages: juvenile, sub-adult and adult (sexual maturity). Sons from biparental families showed (a) reduced anxiety as juveniles; (b) greater exploration and social interaction at different stages; (c) better cognition; and (d) reduced corticosterone concentrations than sons from uniparental families. In contrast, sons from uniparental families showed greater levels of paternal care, although prolactin concentrations did not differ between treatments. Paternal care in striped mice enhances fitness of males. Here, we also show that sons benefit psychologically and physiologically through interactions with their fathers. However, sons also trade-off such benefits against their own paternal care behaviour, suggesting that fathers influence the development of their son's phenotype in complex ways.

Seasonal variation in telomere dynamics in African striped mice.

Telomere shortening has been used as an indicator of aging and is believed to accelerate under harsh environmental conditions. This can be attributed to the fact that telomere shortening has often been regarded as non-reversible and negatively impacting fitness. However, studies of laboratory mice indicate that they may be able to repair telomere loss to recover from environmental harshness, as indicated by recent studies in hibernating rodents. We studied seasonal variation in telomere dynamics in African striped mice (Rhabdomys pumilio) living in a highly seasonal environment. In our annual species, individuals born in the moist spring (high food availability) need to survive the harsh dry summer (low food availability) to be able to reproduce in the following spring. We studied the effect of the harsh dry vs. the benign moist season on telomere dynamics. We also tested if telomere length or the rate of change in telomere length over the dry season predicted the probablity of dissapearance from the population at the same time. Male, but not female, stripped mice showed age-related telomere erosion. Telomeres were longer at the beginning of the dry season compared to the rest of the year. Telomeres increased significantly in length during the moist season. Neither telomere length at the onset of the dry season nor telomere loss over the dry season predicted whether or not individuals disappeared. In conclusion, our data suggest that seasonal attrition and restoring of telomeres also occurs in non-hibernating wild rodents living in hot food restricted environments.

Elevated basal corticosterone levels increase disappearance risk of light but not heavy individuals in a long-term monitored rodent population.

According to the cort-fitness hypothesis, glucocorticoid levels correlate negatively with fitness. However, field studies found mixed support for this hypothesis, potentially because the association between glucocorticoids and fitness might depend on prevailing environmental conditions. Based on the long-term monitoring of a natural rodent population, we tested whether individuals with elevated corticosterone levels were more likely to disappear, accounting for individual condition and among-year variation in food availability, population density and predation pressure. We used basal corticosterone levels measured at the onset of the pre-breeding season in 331 African striped mice from six generations. While basal corticosterone levels were highly repeatable within individuals, between-individual variation was large. Survival analysis revealed that disappearance risk over the pre-breeding season increased with elevated basal corticosterone levels for light but not for heavy individuals. High levels of corticosterone may be more deleterious to smaller individuals (i.e. through allostatic overload), eventually increasing their mortality risk, and disappearance would represent actual death. An alternative non-exclusive explanation could be that high levels of corticosterone selectively trigger dispersal in light individuals, and disappearance would rather reflect their departure from the population. Although environmental conditions varied considerably among generations, none of the interactions between corticosterone and environmental variables were significant. Disappearance probability was positively correlated with both predation pressure and with food availability, a factor favoring dispersal. In sum, elevated basal corticosterone levels increased disappearance in light striped mice, either directly via reduced survival prospects and/or indirectly via dispersal.

Fat content of striped mice decreases during the breeding season but not during the food-restricted dry season.

Individuals that are capable of accumulating appropriate fat stores are assumed to have selective advantages when food becomes scarce. Similarly to species from temperate zones, some species inhabiting arid areas accumulate fat stores prior to periods of food limitation. Yet, we have little knowledge concerning seasonal variation in body composition and the relationship between fat store size and disappearance risk in species from arid habitats. Using the water dilution method, we examined the body composition of African striped mice (Rhabdomys pumilio) living in a seasonal habitat with a long food-restricted dry season. We tested for seasonal changes in body composition (N=159 measurements of 113 individuals) and whether dry season survival was related to fat mass (N=66 individuals). Fat stores were similar in size at the onset and the end of the dry season, but surprisingly smaller at the onset of the moist breeding season. Fat stores showed a negative relationship with food availability. Individual variation in fat stores was not associated with disappearance risk, but there was a positive association of disappearance risk with body mass. Increased disappearance risk of heavy individuals suggests elevated dispersal rates in competitive individuals. This study suggests that non-breeding philopatric striped mice do not accumulate large fat stores prior to the food-limited dry season but that they might mobilize fat stores at the onset of the breeding season to satisfy the energetic demands of reproduction and/or to decrease costs associated with larger fat stores, such as increased predation risk.

Anxiety and exploratory behavior in the African striped mouse, Rhabdomys, taxa are partially modified by the physical rearing environment.

The environment may modulate genetic influences on behavioral expression. We investigated whether the physical rearing environment modulates anxiety and exploratory behavior in four populations, representing three species, of the striped mouse Rhabdomys. One population originated from an arid, open habitat and the others from grassy, covered habitats, and two species occurred in sympatry. We raised captive individuals of all populations in treatments that simulated cover or no cover for two generations and investigated the behavior of resulting adults in an open-field, light-dark and startle response tests. We expected that, when raised without cover, the arid population would be less anxious and more exploratory than grassland populations, but found the opposite in the open-field test only. We also expected that all individuals would be anxious and less exploratory when raised under cover, which was the case for anxiety in a light-dark test, but individuals from the no cover treatment were more anxious in the open-field test. Only one population × treatment interaction was detected in which the arid population was least exploratory. Therefore, the physical rearing environment had less of an influence than phylogeny on the development of anxiety and exploration in Rhabdomys.

Protein deficiency decreases stereotypic behavior frequency and prevalence and activity in the striped mouse Rhabdomys dilectus chakae.

Diverse motivational triggers, including diet, elicit stereotypic behavior. We investigated whether diets comprised of different protein levels but similar levels of energy were associated with the occurrence of locomotor stereotypies in the striped mouse Rhabdomys dilectus chakae. In a first experiment, 20 stereotypic and 20 non-stereotypic (10 subjects per sex and per group) juvenile (40 days old) subjects were placed on baseline (BP), high (HP) or low protein (LP) diet treatments (120 subjects in total). All subjects initially identified as stereotypic displayed stereotypic behavior in the BP and HP treatments on Days 60-63 and Days 80-83 compared to 35% and 12.5% of LP subjects, respectively. Moreover, LP subjects displayed lower levels of activity and stereotypic behavior than BP and HP subjects. Those identified as non-stereotypic never displayed stereotypy. In a second experiment, 48 individuals, bred and reared on LP and whose parents were stereotypic, were assigned to either HP (13 males, 12 females) or LP (12 males, 11 females) treatments at 50 days of age for 30 days. Stereotypy was three times less likely to occur in the LP than the HP treatment, and activity was greater in LP-HP individuals than LP-LP individuals. In both experiments, LP individuals had the lowest body mass. Striped mice adjusted their behaviors in response to dietary protein levels. Protein deficiency reduced activity and stereotypic behavior and prevalence, possibly related to an energy or neurological deficit.

Both thyroid hormone levels and resting metabolic rate decrease in African striped mice when food availability decreases.

In response to variation in food availability and ambient temperature (Ta), many animals show seasonal adaptations in their physiology. Laboratory studies showed that thyroid hormones are involved in the regulation of metabolism, and their regulatory function is especially important when the energy balance of an individual is compromised. However, little is known about the relationship between thyroid hormones and metabolism in free-living animals and animals inhabiting seasonal environments. Here, we studied seasonal changes in triiodothyronine (T3) levels, resting metabolic rate (RMR) and two physiological markers of energy balance (blood glucose and ketone bodies) in 61 free-living African striped mice (Rhabdomys pumilio) that live in an semi-arid environment with food shortage during the dry season. We predicted a positive relationship between T3 levels and RMR. Further, we predicted higher T3 levels, blood glucose levels and RMR, but lower ketone body concentrations, during the moist season when food availability is high compared with summer when food availability is low. RMR and T3 levels were negatively related in the moist season but not in the dry season. Both RMR and T3 levels were higher in the moist than in the dry season, and T3 levels increased with increasing food availability. In the dry season, blood glucose levels were lower but ketone body concentrations were higher, indicating a change in substrate use. Seasonal adjustments in RMR and T3 levels permit a reduction of energy expenditure when food is scarce, and reflect an adaptive response to reduced food availability in the dry season.

Alternative reproductive tactics in female striped mice: Solitary breeders have lower corticosterone levels than communal breeders.

Alternative reproductive tactics (ARTs), where members of the same sex and population show distinct reproductive phenotypes governed by decision-rules, have been well-documented in males of many species, but are less well understood in females. The relative plasticity hypothesis (RPH) predicts that switches between plastic ARTs are mediated by changes in steroid hormones. This has received much support in males, but little is known about the endocrine control of female ARTs. Here, using a free-living population of African striped mice (Rhabdomys pumilio) over five breeding seasons, we tested whether females following different tactics differed in corticosterone and testosterone levels, as reported for male striped mice using ARTs, and in progesterone and oestrogen, which are important in female reproduction. Female striped mice employ three ARTs: communal breeders give birth in a shared nest and provide alloparental care, returners leave the group temporarily to give birth, and solitary breeders leave to give birth and do not return. We expected communal breeders and returners to have higher corticosterone, owing to the social stress of group-living, and lower testosterone than solitary breeders, which must defend territories alone. Solitary breeders had lower corticosterone than returners and communal breeders, as predicted, but testosterone and progesterone did not differ between ARTs. Oestrogen levels were higher in returners (measured before leaving the group) than in communal and solitary breeders, consistent with a modulatory role. Our study demonstrates hormonal differences between females following (or about to follow) different tactics, and provides the first support for the RPH in females.

Seasonal variation in attention and spatial performance in a wild population of the African striped mouse (Rhabdomys pumilio).

Cognitive flexibility describes the reversible changes of cognition in response to environmental changes. Although various environmental factors such as temperature, photoperiod and rainfall change seasonally, seasonal variation in cognitive performance has been reported in merely a few birds and mammals. We assessed whether cognitive performance in a wild population of African striped mice Rhabdomys pumilio, from the Succulent Karoo semidesert of South Africa, differed between summer and winter. In order to measure cognitive performance, striped mice were trapped in the field, tested under laboratory conditions at our research station and returned to the field within 5 h. We measured attention and spatial memory using the standardized orientation response test and the Barnes maze test. Males tested during summer oriented faster toward a predator-stimulus but made more errors and took longer to locate a shelter than males tested during winter. In contrast, females' performance did not differ between the two seasons. We discuss how the faster orientation in males during winter might be the consequence of lower temperatures and/or prolonged food restriction. We suggest that the enhancement of spatial performance during winter might be due to a greater motivation for future dispersal in male striped mice, as spring represents the breeding season.

Alternative reproductive tactics in female striped mice: heavier females are more likely to breed solitarily than communally.

Alternative reproductive tactics (ARTs) are discrete reproductive phenotypes governed by decision rules called strategies. ARTs are fixed for life in species with alternative strategies, while tactic expression is plastic in species with a single strategy. ARTs have been investigated in males of many species, but few studies have tested whether the same theoretical framework applies in females. Female striped mice (Rhabdomys pumilio) employ three ARTs: communal breeders give birth in a nest shared with female kin and a breeding male and show allo-parental care; returners give birth away from the shared nest and later return to it; and solitary breeders give birth away from the shared nest and do not return to the group. Here, studying free-living female striped mice over six breeding seasons, we tested whether ARTs arise from alternative strategies or a single strategy. We also asked to what extent stochastic extrinsic factors explain whether individuals become solitary rather than group living. Females switched tactics, consistent with a single strategy, so we tested whether this represented a mixed or conditional single strategy. Only the latter predicts differences between ARTs in traits indicating competitive ability, such as body mass or age, before individuals adopt a tactic. We weighed females at conception when they were still group living to eliminate potential confounding effects of gestation and subsequent social tactic (solitary versus group living) on body mass. Females that went on to use a solitary ART were heavier than those that became communal breeders and returners, in support of a conditional strategy. Solitary breeders also arose through extrinsic factors (mortality of all adult female group members). They weighed less than females that became solitary while relatives were alive, but did not differ in body mass from communal breeders and returners. We conclude that ART theory applies to both sexes, with female striped mice following a conditional single strategy. Future studies should consider the possibility that phenotypes that superficially resemble evolved tactics might also arise through non-adaptive extrinsic causes.

Basal blood glucose concentration in free-living striped mice is influenced by food availability, ambient temperature and social tactic.

Vertebrates obtain most of their energy through food, which they store mainly as body fat or glycogen, with glucose being the main energy source circulating in the blood. Basal blood glucose concentration (bBGC) is expected to remain in a narrow homeostatic range. We studied the extent to which bBGC in free-living African striped mice (Rhabdomys pumilio) is influenced by ecological factors with a bearing on energy regulation, i.e. food availability, abiotic environmental variation and social tactic. Striped mice typically form extended family groups that huddle together at night, reducing energetic costs of thermoregulation, but solitary individuals also occur in the population. We analysed 2827 blood samples from 1008 individuals of seven different social categories that experienced considerable variation in food supply and abiotic condition. Blood samples were taken from mice in the morning after the overnight fast and before foraging. bBGC increased significantly with food plant abundance and decreased significantly with minimum daily ambient temperature. Solitary striped mice had significantly higher bBGC than group-living striped mice. Our results suggest that adaptive responses of bBGC occur and we found large natural variation, indicating that bBGC spans a far greater homeostatic range than previously thought.

Separation at weaning from the family is stressful for naturally group-living, but not solitary-living, male African striped mice Rhabdomys.

Early separation from a family is stressful for young mammals, but might be more stressful for group-living than solitary species. Using juvenile males of three African striped mice Rhabdomys taxa that are either group (R. pumilio) or solitary (R. dilectus dilectus and R. d. chakae) living, we predicted greater separation anxiety in R. pumilio than R. dilectus because group-living could reduce anxiety in R. pumilio. Three brothers from each of 10 litters per taxon were randomly assigned soon after natural weaning (25 days) to one of three treatments for 10 days: (1) remained with the family (philopatric); (2) separated from the family by a wire mesh barrier (separated); and (3) isolated from the family (isolated). Males were individually tested in a four-arm maze to assess their anxiety responses and sampled for corticosterone concentrations 20 mins and 10 days later. Compared to R. dilectus males, R. pumilio males showed a greater treatment response to separation: philopatric males used the light arms of the maze less and had higher corticosterone concentrations compared to isolated males, which spent the most time in the light arms and had the lowest corticosterone concentrations overall; separated males showed an intermediate behavioural response, but had similar corticosterone concentrations to philopatric males. Thus, separation from a family group is more stressful in group-living Rhabdomys and this stress response dissipates with time. Philopatry and group-living may be more important for young R. pumilio, whereas dispersal at weaning is an important life history event for solitary R. dilectus.

Behavioral responses of vervet monkey Chlorocebus pygerythrus infants in a novel fostering program.

Vervet monkeys (Chlorocebus pygerythrus) are considered pests by farmers and homeowners. Consequent attempts to exterminate problem adult vervet monkeys often result in orphaned young offspring, which are sometimes taken to wildlife rehabilitation centers. We assessed the success of a novel fostering program at the Vervet Monkey Foundation, South Africa. Nine orphaned vervet monkeys were fostered to adult conspecific females of existing troops at the Foundation. The fostering protocol focused on reducing the time orphans spent in human rearing and involved a stepwise process of integration. We recorded the behaviors of orphans, including their interactions with their foster mother, to assess the process of fostering. Fostering success was high (89%). Orphans maintained close association with the foster mother and had little or no socio-negative and abnormal behavior. Comparison with literature showed a similar high fostering success in another vervet monkey study, regardless of the period and level of human-caregiving, and it is apparent that the duration of human care is less important than the protocol used for fostering. Nonetheless, our study has conservation relevance for vervet monkey rehabilitation.

Wild mice in an urbanized world: Effects of light at night under natural and laboratory conditions in the single-striped grass mouse (Lemniscomys rosalia).

Urbanization, and the accompanying artificial light at night (ALAN), can disrupt the activity of animals. Such disruptions at the base of a food web can ripple through the ecosystem. Most studies of ALAN are performed in the laboratory. Thus, we lack basic information about the circadian responses of animals under natural environmental conditions to fully evaluate the impact of ALAN. We studied the behaviour and activity of wild-caught, peri-urban single-striped grass mice (Lemniscomys rosalia) under a natural treatment and in a standard laboratory treatment, including dim light at night to mimic conditions that they could experience. The species exhibited predominantly crepuscular activity under all experimental treatments. It showed the highest level of activity under the natural treatment, whereas ALAN significantly suppressed its activity. Males were more active than females under all experimental treatments. The marked changes in activity under ALAN is of particular concern since global change in combination with urbanization can lead to a change in vegetation density and composition that will decrease the number of suitable microhabitats and expose small mammals to novel habitat changes. We suggest that the single-striped mice could become vulnerable because of urbanization, leading to impacts on its ecosystem broadly.