The Striped Mouse: Ideal Model to Study Paternal Care, Reasons for Group Living and Social Flexibility
By Carsten Schradin
· Distribution and Characteristics
· A group living solitary forager in the succulent karoo
· Communal nesting and paternal care
· Potential reasons for group living
· High population density
· Short breeding season
· Other habitats - other habits: The striped mouse in the grasslands
· Social flexibility in the Succulent Karoo
· Physiological flexibility and adaptation to droughts, one consequence of climate changes
· Why research on the striped mouse?
Distribution and Characteristics
Apart from humans, the striped mouse (Rhabdomys spec.) is probably the most common mammal in Southern Africa. There are now at least two specie recognised (Rhabdoms dilectus from the moist graslands and Rhabdomys pumilio, the species we study). The distribution of the specieshich ranges even within East Africa, where it is mainly restricted to high attitudes, e.g. Mt. Kilimanjaro in Tanzania. This genus is so wide spread, because it can live in a wide range of different habitats: Green and moist grasslands, the Kalahari and the Namib desert, Karoo and Succulent Karoo, mountain areas and even at the edge of forests. The striped mouse got its name from four dark stripes on its back, separated by three lighter, sometimes even white stripes.
A group living solitary forager in the Succulent Karoo
I did my PhD thesis about paternal care in New World monkeys. I thought this is a very interesting topic, but primates are an expensive model where it is difficult to get good sample sizes, especially when working in the field. As I found some evidence in the literature that the striped mouse might show paternal care, I went as a postdoc to South Africa to investigate this. I soon found out that this species is in fact highly paternal, with males showing the same parental behaviour patterns as females and to the same extend, with the obvious exception of nursing. However, this was in captivity, and could have been an artefact of the unnatural conditions under which the animals had been kept. In fact, the striped mouse had been studied for decades in the moist grasslands of South Africa, and seemed to be a solitary species. Males were thought to search for females to mate with them, but not to participate in parental care. However, as the striped mouse occurs in many different habitats, I decided to study it in the wild in a habitat very different from the moist grasslands: In the Succulent Karoo, a semi-desert to desert in the North West of South Africa. As study site I chose the Goegap Nature Reserve near Springbok, because another scientist, Tim Jackson from the University of Pretoria, had studied whistling rats there and reported that striped mice are common in this reserve.
The results I got within five months were astonishing: One of the most complex and interesting social systems described for rodents. The mice were group-living, tThey shared one nest in a shrub and in the morning I could see up to 30 adult mice of both sexes at their nest. They interacted highly amicable with each other, sitting in body contact or grooming each other. Then, after about 20-30 minutes of basking in the sun, they left. Not as a group, but every mouse into another direction. During the day they were foraging alone, and met again during the late afternoon at their nest. Here they greeted each other by sniffing at each other and they basked in the sun, before withdrawing into the nest. When two mice met during the day, they did not pay much attention to each other when they were from the same group. However, when the mouse was from another group, it was chased away aggressively. Males were especially aggressive against other males, while females chased males as well as other females. Mice were highly aggressive when they encountered a stranger that was smaller than them, while a bigger mouse at the territory boundary was not attacked. However, in front of their nests strangers even double the size were immediately taken care of and chased out of the territory.
Communal nesting and paternal care
Groups typically consisted of one breeding male and up to four breeding females. The male was highly sociable, showing as much social interactions with juveniles as females did. They even retrieved pups presented in front of their nest into their nest. Videotaping inside natural nests indicated that the males were sleeping with the rest of the group, and that they showed parental care in the nest. Thus, our observations of paternal care in captivity were no laboratory artefacts, also occurs in the field.
A group has 2-4 breeding females. These females originate from the same group, which means they are closely related such as sisters or half sisters, while the breeding male originates from another group. All or most adult females of a group give birth and are raised together. Sometimes a female leaves the group nest to give birth elsewhere and only returns with the pups when those are around 10 days old. The offspring remains in their natal group even after reaching adulthood. This is the case both for males as well as for females. Interestingly, these offspring normally do not start to reproduce themselves, even when they are sexually mature and the breeding season is not yet over. Both juvenile and adult offspring help in nest construction, territory defence and warming younger pups in the nest. This why they are called helpers at the nest.
Potential reasons for group living
The striped mouse in the Succulent Karoo can best be describes as a territorial group living solitary forager with communal nesting, paternal care and helpers at the nest. Why did such a complex social system evolve?
There are two reasons for this complex social system: 1. High population density leading to habitat saturation and forced philopatry, and 2. short breeding season leading to the absence of reproductive competition for most time of the year.
High population density
After the breeding season, more than 200 striped mice can live per hectare. This means the territories of groups are very small, only 0.1 to 0.3 ha, or 10x10 to 18x18 meters. Groups within such territories consist of 8-30 adult mice, and each territory is surrounded by other territories, which are also heavily packed with mice. As mice travel between 300 and 1000 meters a day and because it is such a small area, they often encounter mice from other groups. Such encounters are typically aggressive, and juveniles have only one choice when meeting an adult and thus much larger stranger: Run away as fast as possible! This means, young mice learn very quickly that there is no place where they can go to, they have to stay at home! The stressful encounters with aggressive mice from other groups are also the reason why adult offspring do not start to show signs of reproduction.
But why is the population density so high? This is so because the survival probability of mice is extraordinarily high. More than 30% of the mice can survive for more than one year. 30% might sound small, but for a small mammal this is very high. The same species in the grasslands has an annual survival probability ten times smaller, with only about 3% surviving for more than one year. And the reasons for this good survival in the Succulent Karoo are good food availability and benefits of group living.
The Succulent Karoo is dry, with only 150mm of rain a year at my field site. Accordingly, plant cover is low. But in spring after the winter rains most of the land is covered by short living plants, especially wildflowers, but this lasts only for three months. Afterwards shrubs and succulents dominate the landscape, but a large amount of the soil simply consists of plain sand. So one might think the mice might have a problem to find food. However, although there is not much growing, nearly everything that is growing, is mouse food. Of 51 plant species at my field site, 32 are eaten by the mice. And during spring there is more than enough food available, and the mice get really fat. The heaviest striped mice ever have been trapped at my field site (over 80g, both for males and for females). During the following dry summer they loose 12% of body mass, but that simply means they arrive at a body mass normal for other populations. Then the autumn rains start and new mouse food is growing.
Living in a group has also advantages that increase the survival probability of mice. First they share one nest, and the sleep closely huddled together. Even in summer nights it can get relatively cold in the Succulent Karoo, down to only 10 degrees, which is not much for a small mammal. In winter frost is common. The mice form a real ball of mice in the nest, warming each other. By this they reduce energy loss and thus save energy themselves. While videotaping wild mice over entire nights in time-lapse mode, I found that not all mice are sleeping at the same time. A mouse nest never gets really quiet, not even after midnight. This probably serves as a warning system, as the approach of a potential predator is more easily realized when one the group members is always awake and serves as a sentinel. The nests are built from hay and are above ground inside shrubs. Thus, they are relatively easily accessible for snakes. While a single (sleeping) mouse might not realize when a snake approaches during the night, a group of several mice with one always awake will easily realize when a predator approaches and flee out of the nest.
Short breeding season
The seasons in the Succulent Karoo are dictated by the rain that occurs in winter. Winter is pretty cold, with temperatures below zero, which might explain why breeding of the striped mice (and most other animals) only starts in spring. Spring is characterized by a high percentage of plant cover, mainly wildflowers and herbs. In September (spring on the southern Hemisphere), Namaqualand is covered in a colourful coat of yellow, blue and orange, the colours of hundreds of species of wildflowers. However, this richness is of short duration, and in November the country turns desert again. The short season of the plenty determines also the breeding season of the mice. The breeding season is only 3 months long, enabling females to get 2-3 litters. Mice get sexually mature when they are only around 6 weeks old and have a body weight of 25g, although they still grow for several weeks until they reach a body weight of 40-50g. However, in the Succulent Karoo this means that when a mouse gets sexually mature, the breeding season is nearly over. Habitat saturation forces them to stay at home. At the end of the breeding season, when most mice born during that year are still juveniles, reproductive competition between group members reaches zero. As the breeding season is terminated, nobody breeds, and there is no potential for competition over breeding status between group members. Thus, at this stage staying in the natal group is not associated with any costs or conflict due to reproductive competition, but mice can enjoy benefits of group-living.
Other habitats - other habits: The striped mouse in the grasslands
In the Succulent Karoo, the striped mouse is living in complex social groups. This result was surprising, as many previous studies in grasslands have reported a solitary lifestyle for the same species (which by now is described as a different species, Rhabdomys dilectus instead of Rhabdomys pumilio). However, there was one important difference between previous studies and my study: Other studies totally relied on capture-mark-recapture, i.e. researchers trapped mice, marked them, and looked where else the same individuals were trapped. Using radio-telemetry, I compared Rhabdomys pumilio from the Succulent Karoo with Rhabdomys dilectus living 800kms away in the moist grasslands of the Drakensberge in the Kamberg Nature Reserve. With this study I could conform that striped mice from grasslands are solitary, which is in contrast to the group-living striped mice from the Succulent Karoo.
Social flexibility in the Succulent Karoo
We suspected high population density due to a high survival probability and the short breeding seasons as the reasons for group living in the Succulent Karoo. In contrast, population density in the grasslands is much lower, only around 10 mice/ha compared to 40 mice/ha in the Succulent Karoo at the start of the breeding season. This is because the annual survival probability of 2% is ten times smaller than that of the Succulent Karoo. Also, while the breeding season in the Succulent Karoo is 3 months short, it is 7 months long in the grasslands. Thus all of this fitted nicely into our explanations.
But as scientists we would have liked to test some predictions. Our predictions would have been that when we get the same situation in the Succulent Karoo as in grasslands, the social system of the mice should change. More precisely: Low survival probability resulting in low population density in the Succulent Karoo would resemble the situation in grasslands and lead to a solitary lifestyle.
When I came back to Goegap in 2003, it was not my intention to test these predictions. I had marked more than 200 mice the year before and studied 9 social groups. I was anxious to see how these groups had developed. Would the females born in one group in 2002 stay together in 2003 and form communal nests? What factors would determine which females stay together, who left? Who had survived? Would the males emigrate into other groups? What happens to males that do not find a group?
I soon found out how my study groups had developed: They were all extinct! Of the more than 200 marked mice, only 4 had survived. The winter of 2003 experienced the severest drought in recorded history (since 1960), most mice had died. It was totally dry, no mouse food was available, and the few survivors were just skin and bones. Finally, we got rain at the end of winter in August, and plenty of it. After the rain, icy cold air was coming from the Antarctic, it was freezing every night. As a consequence, every second of the few survivors died in the cold.
My situation was frustrating and depressing. Nearly all my study animals were gone. What to do?
After I had relaxed and send my depressions over the mountains, I realized that this catastrophic disaster enabled me to test the prediction whether low population density leads to a solitary lifestyle. I expanded my field site from 3 ha to 40ha, and by this managed to trap enough mice to study them.
The results were clear. In 2003, all the females in the Succulent Karoo became solitary, and so did the males. Like in the grasslands, the males had now much larger territories than females, and they overlapped the territories of several females. The drought had minimized survival probability, reduced population density and changed the social system from group to solitary living.
And the second factor, the duration of the breeding season? Like in other years, the breeding season was again only 3 months long in the Succulent Karoo. If the lack of reproductive competition due to a short breeding season would favour group living, one would predict that groups form again. And this is exactly what we observed. At the end of the breeding season family groups established again. As the population density at this stage was much lower than in previous years and even lower than in grasslands, this also indicated that it is not only the population density alone that dictated the social system: The presence or absence of reproductive competition is itself an independent important factor.
Collecting data over many years, we found a significant correlation between population density and sociality, but only during the breeding season: the lower the population density, the more mice were solitary. Outside the breeding season, when no reproductive competition occurs, mice were always group-living, independent of population denisty. My PhD student Ivane Schoepf confirmed this experimentally: she removed mice from the field, locally reducing population density. Only duirng the breeding season did this influene sociality, but not during the dry season.
Physiological flexibility and adaptation to droughts, one consequence of climate change
The striped mouse shows extraordinary flexibility in its social system, enabling it so suirvive in an extreme and variable environment. This flexibility is partly regulated by hormones, especially prolactin, testosterone and corticosterone. However, hormones do not primarily have the function to regulate behavior, but physiology: osmoregulation, reproduction and especially metabolism. In a period of food shortage in the dry season, striped mice have to save energy. We are currently studying physiological flexibility as an adaptation to droughts, which in the future will occur more often and become more severe due to climate change. Apart from hormones we measure the metabolic rate of striped mice and their daily energy expenditure. We are especially interested in studying how the physiology of survivors differs from that of mice that die during the dry season, and which external factors (age, body mass, sex, social status) influence this.
Why research on the striped mouse?
Why do research on striped mice? Why spend so much time, energy and money for studying the social behaviour of such a small rodent in southern Africa? There are three good reasons why to do so:
1. This research and its results are very fascinating. For many people, the results are interesting and they are surprised to learn about how complex and complicated the life of such a small mammal can be. Behavioural biology as such is a kind of and contribution to our culture, as are the arts. Many people like to go to the opera, just as many people are interested in nature. Here it does not matter that not everybody goes to the opera or is interested in nature, but it matters that many do.
2. The striped mouse is a very good system to understand human behaviour. One might say that to understand humans one should better study their closest relative, apes and monkeys, and compare them with us. However, the mice share one characteristic with us that most primates do not have: Social flexibility. Most primate species have a relatively fixed social system, such as living in family groups (titi monkeys and gibbons), harems (colobus monkeys and gorillas) or in multi-male multi-female groups (baboons and chimpanzees). In contrast, humans are very flexible. In our species you find monogamy, polyandry and polygyny. People can live in small nuclear families or in extended families, in small groups or alone. No other primate has this social flexibility, but the striped mouse has it. Like in humans, some males are good fathers, others leave the mother which has to raise the offspring alone.
3. The striped mouse offers an ideal system to study behavioral and physiological adaptation to extreme environment, especially droughts, one of the consequences of climate change. By understanding how striped mice can cope with unpredictable droughts, and especially understanding why many individuals cannot and die, we can make predictions for other species that will have to cope with droughts in the future. We are lucky to have an animal model that enables us to study these consequences - an animal that lives for not much more than a year, not decades, such that we can compare data of many generations living under different environments.
However, my main motivation to study these animals is simply that it is fascinating. What we observe in Goegap is a soap opera of the most exciting kind. Every individual has its own life history, experiences good and bad times during its life. We are often astonished how similar the mice are to us. Of course it would be wrong to humanize the mice, but their life histories are nevertheless interesting. Below you can read about the lives of different individuals in the "mouse portraits". You can decide for yourself whether these mice have interesting lives or not.
|Juvenile striped mice.
|A group of mice are basking in front of their nest. We mark mice individually with hair dye. Colours at the back indicate males, at the front females. In front you see male 33 and female 23.
|A wild male (right) takes care of a pup that has been experimentally presented to him in front of his nest. One juvenile male (front) is also interested, while two more juveniles (back) are watching from a distance.
|The pups leave their nest (here an abandoned whistling rat burrow) already at an age of 10-12 days, but first only to bask in front of it. At an age of 16 days they leave the nest for foraging.
|The vegetation of the grasslands in South Africa is very different from the Succulent Karoo. Although it looks nicely green, there is little food for mice, which cannot digest grass.
Home ranges of striped mice (Rhabdomys pumilio) in the Succulent Karoo: lots of overlap because of group-living and high population density.
Home ranges in the grasslands are much larger and overlap little. Here striped mice (Rhabdomys dilectus) are solitary living.
Data from 8 years of long-term field studies. In the breeding season (grey diamonds) there is a significant correlation between population density and sociality, with more mice being solitary when popultaion density is low. Outside the breeding season (black dots and stars) mice are always group-living, even when population density is low (far left).
Experimentally reducing population density lead to the same results as the descriptive field study: mice become solitary during the breeding season (line) but not duirng the dry season.
During the dry season (right) striped mice have much lower corticosterone levels than during the breeding season. Corticosterone is an important metabolic hormone and decreasing corticosterone during the dry season probably helps reducing energy expenditure.
The striped mouse is an ideal model to study highly interesting aspects of social behaviour: Paternal care, communal nesting, group living and social flexibility. It also tells us how behavioral and physiological flexibility enables survival in a changing world.
However, simply to study their individual live histories is extremely interesting and it is astonishing to see how individuals even have different personalities.