Tasmin L. Rymer

Behavioural correlates of urbanisation in the Cape ground squirrel Xerus inauris

Urbanisation critically threatens biodiversity because of habitat destruction and novel selection pressures. Some animals can respond to these challenges by modifying their behaviour, particularly anti-predator behaviour, allowing them to persist in heavily transformed urban areas. We investigated whether the anti-predator behaviour of the Cape ground squirrel Xerus inauris differed in three localities that differed in their level of urbanisation. According to the habituation hypothesis, we predicted that ground squirrels in urban areas would: (a) be less vigilant and forage more; (b) trade-off flight/vigilance in favour of foraging; and (c) have shorter flight initiation distances (FID) when approached by a human observer. Observations were made in winter and summer at each locality. As expected, ground squirrels in urbanised areas were less vigilant and had shorter FIDs but did not trade-off between foraging and vigilance. In contrast, a population in a non-urbanised locality showed greater levels of vigilance, FID and traded-off vigilance and foraging. A population in a peri-urban locality showed mixed responses. Our results indicate that Cape ground squirrels reduce their anti-predator behaviour in urban areas and demonstrate a flexible behavioural response to urbanisation.

Behavioural divergence, interfertility and speciation: a review.

Behavioural compatibility between mates is fundamental for maintaining species boundaries and is achieved through appropriate communication between males and females. A breakdown in communication will lead to behavioural divergence and reduced interfertility. In this review, we summarise the current knowledge on male signals and female perception of these signals, integrating the literature from several taxa. We advocate that signaller-perceiver coevolution, which is usually under strong stabilising selection to enable mating, forms the basis of species-specific mate recognition systems. The mechanisms (phylogeny, geography, ecology, biology) shaping signaller-perceiver systems are briefly discussed to demonstrate the factors underpinning the evolution of signaller-perceiver couplings. Since divergence and diversification of communication systems is driven by changes in the mechanical properties of sensory pathways and morphology of sensory organs, we highlight signal modalities (auditory, olfactory, visual, tactile) and their importance in communication, particularly in mate selection. Next, using available examples and generating a stylised model, we suggest how disruption (biological, ecological, stochastic) of signaller-perceiver systems drives behavioural divergence and consequently results in reduced interfertility and speciation. Future studies should adopt an integrative approach, combining multiple parameters (phylogeny, adaptive utility of communication systems, genetics and biomechanical/biochemical properties of signals and perception) to explore how disruption of signaller-perceiver systems results in behavioural divergence and reduced interfertility. Finally, we question the impact that rapid environmental change will have on disruption of communication systems, potentially interfering with signaller-perceiver couplings.

The Development of Exploratory Behaviour in the African Striped Mouse Rhabdomys Reflects a Gene × Environment Compromise

Behaviour results from the interaction of an individual’s genotype with prevailing environmental conditions, resulting in local adaptation to specific habitats. We investigated the development of exploratory behaviour in two closely-related species of African striped mice from the semi-arid Succulent Karoo (Rhabdomys pumilio) and moist grassland (R. dilectus chakae) localities. Irrespective of sex, R. pumilio displayed greater exploratory behaviour (open field) and greater use of the open arms of a modified plus maze, and thus were less anxious and bolder than R. d. chakae. When pups were cross-fostered between species, fostered individuals of both species showed an intermediate behavioural pattern between their foster and biological siblings: fostered R. pumilio explored more than their foster siblings but less than their biological siblings, whereas fostered R. d.chakae explored more than their biological siblings, but less than their foster siblings. Our study is one of the first to address how the underlying genotype and early postnatal experience interact to influence the expression of exploratory behaviour and personality. In particular, we showed that, in striped mice, the early postnatal environment shapes the anxiety responses and concomitant exploratory behaviour, but the genotype apparently modulates the phenotype and constrains the limit of behavioural flexibility.

Transmission of parental care behavior in African striped mice, Rhabdomys Pumilio.

The expression of behavior, including parental care behavior, is influenced by complex interactions of the genes of an organism and the prevailing environmental conditions. Previously, we showed that the development of paternal, but not maternal, care in the African striped mouse, Rhabdomys pumilio, has a significant nongenetic maternal component. Here, we investigate the genetic component of parental care behavior from parents to offspring. We first measured the duration of parental care behavior of mothers and fathers every second day for 11 days postnatally. Subsequently, one son and one daughter from each of these litters were paired with unrelated mates when they were adults and their parental care behavior scored. Using regression models, we then compared parental care behavior of parents and their adult offspring. The transmission of parental care behavior from striped mouse fathers to sons and from mothers to both sons and daughters did not indicate a genetic component. Instead, we found a patrilineal genetic component for parental care in daughters. The reason for this unusual pattern of inheritance is not known, but this finding complements that of our other studies, showing that the expression of maternal care behavior in adult daughters is also not nongenetically influenced by their mothers. We suggest that, although females are constrained to provide maternal care in different social contexts, maternal care behavior may be influenced genetically by the father.

Resilience to Droughts in Mammals: A Conceptual Framework for Estimating Vulnerability of a Single Species

The frequency and severity of droughts in certain areas is increasing as a consequence of climate change. The associated environmental challenges, including high temperatures, low food, and water availability, have affected, and will affect, many populations. Our aims are to review the behavioral, physiological, and morphological adaptations of mammals to arid environments, and to aid researchers and nature conservationists about which traits they should study to assess whether or not their study species will be able to cope with droughts. We provide a suite of traits that should be considered when making predictions about species resilience to drought. We define and differentiate between general adaptations, specialized adaptations, and exaptations, and argue that specialized adaptations are of little interest in establishing how nondesert specialists will cope with droughts. Attention should be placed on general adaptations of semidesert species and assess whether these exist as exaptations in nondesert species. We conclude that phenotypic flexibility is the most important general adaptation that may promote species resilience. Thus, to assess whether a species will be able to cope with increasing aridity, it is important to establish the degree of flexibility of traits identified in semidesert species that confer a fitness advantage under drying conditions.

Habitat complexity, environmental change and personality: A tropical perspective.

Tropical rainforests are species-rich, complex ecosystems. They are increasingly being negatively affected by anthropogenic activity, which is rapidly and unpredictably altering their structure and complexity. These changes in habitat state may expose tropical animals to novel and unpredictable conditions, potentially increasing their extinction risk. However, an animals ability to cope with environmental change may be linked to its personality. While numerous studies have investigated environmental influences on animal personalities, few are focused on tropical species. In this review, we consider how behavioural syndromes in tropical species might facilitate coping under, and adapting to, increasing disturbance. Given the complexity of tropical rainforests, we first discuss how habitat complexity influences personality traits and physiological stress in general. We then explore the ecological and evolutionary implications of personality in the tropics in the context of behavioural flexibility, range expansion and speciation. Finally, we discuss the impact that anthropogenic environmental change may have on the ecological integrity of tropical rainforests, positing scenarios for species persistence. Maintaining tropical rainforest complexity is crucial for driving behavioural flexibility and personality type, both of which are likely to be key factors facilitating long term persistence in disturbed habitats.

Maternal care in the African striped mouse Rhabdomys pumilio: A behaviorally flexible phenotype that is modified by experience

The development of maternal care in mammals can be influenced by the type and quality of maternal care received. Using biparental striped mice Rhabdomys pumilio, we investigated whether development of maternal care is influenced by the mother during early rearing and by an adult females experience and that of her mate. Offspring were raised in one of three treatments, by: both parents; mothers alone; and mothers separated from the father with a barrier. Since female striped mice increase their care when raising litters alone, which influences expression of parental care of their adult sons, we expected daughters to respond like sons. However, there was no treatment effect in the development of maternal care in daughters. In subsequent experiments, experienced and inexperienced females decreased care when raising their offspring with experienced but not inexperienced males. Therefore, maternal care in striped mice is modulated in response to prevailing environmental and social conditions.

Pre- and postnatal dietary protein deficiency influences anxiety, memory and social behaviour in the African striped mouse Rhabdomys dilectus chakae.

Dietary protein deficiency influences the behavioural phenotypes of mammals. We studied whether protein deficiency during gestation and/or post-weaning heightened anxiety, reduced memory recall and influenced competitive ability in the African striped mouse Rhabdomys dilectus chakae. Mice were subjected to five protein diet treatments, which they received continuously, or were raised on one diet to weaning and switched to an alternate diet post-weaning (Day 16): 1) HP-HP: high protein (24%); first letter pair indicates maternal diet and the second pair indicates offspring diet post-weaning; 2) BP-BP: baseline protein (19%); 3) LP-LP: low protein (10%); 4) HP-LP: switched from high to low protein diet; and 5) LP-HP: switched from low protein to high protein diet. From Day 70, when mice were sexually mature, 20 individuals (10 males, 10 females) per treatment were subjected to three successive experiments, in which we tested their anxiety responses in: 1) an open field arena (time spent in the centre of the open field); 2) novel object recognition (time spent exploring a novel object); and 3) social interactions (excluding BP-BP) in age-matched same-sex dyadic encounters (aggressive, amicable and avoidance behaviours). LP-LP and LP-HP treatment mice spent the least amount of time in the centre of the open field, did not demonstrate object preference compared to the other treatments, and were the most aggressive in dyadic encounters. Our study shows that the systemic effects of protein-deficient diets during early life shapes the behavioural phenotype in R. d. chakae, possibly through early organisation of neuro-biological pathways or competition among littermates.

Alloparenting enhances the emotional, social and cognitive performance of female African striped mice, Rhabdomys pumilio

Maternal care, either of a females own biological offspring or of fostered young, alters the behavioural, endocrine and brain functions of rodents. We asked whether female African striped mouse alloparents (i.e. those assisting in raising their younger siblings) are similarly influenced. We tested whether alloparental care enhances factors of ecological importance by assessing the emotional response, social competitive ability and spatial learning and memory of age-matched, sexually mature females assigned to one of five treatments based on their housing arrangement: housed with their mothers (Alloparents), housed with their mothers, but did not raise a litter (Resident), separated from their mothers and younger siblings with a barrier (Barrier), housed alone (Alone) and primiparous breeders (Breeder). Ten females per treatment were subjected to a range of behavioural tests from 125 to 145 days of age. Breeders and Alloparents were indistinguishable in displaying greater disinhibition of novelty in open field tests, improved competitive ability during social interactions and improved spatial memory in the Barnes maze. Females that did not encounter pups (Resident, Barrier, Alone) did not show such enhanced abilities. These tests indicate that females that raise their own biological pups or help others to raise young benefit through better foraging skills and lowered anxiety in novel situations. Ultimately, alloparents derive direct benefits by improving their parental and foraging skills, in addition to indirect inclusive fitness benefits of caring for their young siblings.

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

Abstract 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.