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 also in the Succulent Karoo
· Future studies
· Why research on the striped mouse?

Mouse Portraits

Distribution and Characteristics

Apart from humans, the striped mouse (Rhabdomys pumilio), also called the four-striped mouse or even the four-striped grass mouse, is probably the most common mammal in Southern Africa. Its distribution ranges even within East Africa, where it is mainly restricted to high attitudes, e.g. Mt. Kilimanjaro in Tanzania. This species 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. It got its name from four dark stripes on its back, separated by three lighter, sometimes even white stripes. The basic colour is brown that ranges from very light to very dark. However, geographical differences in brown darkness might be due to environmental, not genetic differences. For example striped mice in the Succulent Karoo are much darker than in the grasslands of Kwa-Zulu Natal, but in captivity there is no difference. For a mouse species the striped mouse is medium sized, about 30-40g as adults, although large individuals can weight over 80g, in captivity even more. As such, it is about double the size of a house mouse. However, in contrast to this species the striped mouse is diurnal, being active during the day. In winter mice are active during the entire day, while in summer the mice rest during the hot parts of the day and are mainly active during the morning and late afternoon. The striped mouse is the only species of its genus Rhabdomys, although recently it had been proposed that it actually consists of two sister species, one inhabiting the arid areas of the east and the other one the moist grasslands of the west. There are clearly genetic differences between these populations, which is not surprising as they are more than 1000 kms apart from each other. However, in how far these differences justify the nomination of a new species is still under debate.

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, at least I was very surprised by what I found: One of the most complex and interesting social systems described for rodents. The mice were group living in Goegap. They shared one nest in a shrub and in the morning I could see up to 30 adult mice of both sexes leaving their nest, basking in front of it. 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 hereby 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 two 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, but male parental care 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 often more than 10 juveniles of about the same size can be observed in front of a nest. As a female normally gets only 5 pups, these juveniles must have had at least two mothers. Sometimes a female leaves the group nest to give birth elsewhere and only returns with the pups when those are around 10 days old. But in other cases it seems that more than one female gives birth in the same nest and that females rear their offspring communally. 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. Thus, they can be 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 likely 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 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 further found out that they are not sleeping very tight. In fact, at least one group member seems to be relatively awake all the 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 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 0, 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 (inter-birth interval minimum of 23 days). Mice get sexually mature when they are only 6-8 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. One reason why juvenile and adult offspring staying at home show helping behaviour is simply because this comes at no great costs. Helping to build a nest means they also build their own nest, and warming and huddling pups during the night means at the same time they warm themselves. So far we do not know whether helpers increase their time in the nest during the day when pups are present, which would be a real cost. Defence of the group territory and nest is clearly a dangerous behaviour, but again the individual itself benefits directly. Thus, helping behaviour of striped mice can to a large extend be explained by direct individual benefits. Similarly male parental care can be explained by its low costs. Males are associated to groups of 2-4 breeding females. They monopolize these groups by aggressively chasing away all strange males from their territory. Neighbouring groups of communally nesting females are defended by other males, and no male can defend more than one group of females. Thus, the male spends all its time at the nest of his group of communally nesting females. And this is where the pups are. As the male is at the same place as the pups, it does not cost him any time to take care of them. His main contribution might be warming the pups, and his presence positively influences the development of pups. He contributes as much as females to raise the pups, the high energetic costs of lactation not taken into account. Males also visit the nest during the day, which might be costly, as he cannot defend his territory during that time. But the main reasons for paternal care can be seen in its low costs, as males are anyway associated with pups, and its resulting benefit, i.e. improved development of pups.

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. 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. In contrast, I used direct observations. As in the Succulent Karoo the striped mouse is group living but a solitary forager, I wondered whether previous studies in grasslands got the wrong impression. Thus, I had to go there and investigate myself. Of course direct behavioural observations in the grasslands are impossible: the vegetation is much too dense. So I had to find another method to compare the two populations, and the method of choice was radio-tracking. Mice got some radio-transmitters on, and we determined their home ranges. The question was whether several mice overlap their home ranges, i.e. form groups, or have excusive home ranges. We intruded even more into their privacy and radio-tracked them at night, to see whether they were sleeping alone or in groups. To work in the grasslands I went to Kamberg Nature Reserve in the Drakensberg mountains of Kwazulu Natal, South Africa. This is more than 800km away from Goegap as the jackal buzzard flies, but for my car it was more than 1300kms. It was exciting to live for some months in a habitat that is totally different from Goegap. It was summer and raining nearly every day. The vegetation was flourishing, everything was green. One should think such a green land must be a heaven for the mice, but it is not. Mice are not cows, they cannot digest grass! Instead they feed on grass seeds, herbs and berries, and this food is widely distributed and sparse. This might explain our surprising results from radio-tracking: The territories of females in the grasslands were 6 times larger than those of females in the Succulent Karoo. Furthermore, this territory was not shared with any other mice and the females normally slept alone. Only sometimes they were visited by a male, but only for a few nights, not permanently. The males had even larger home ranges than the females. Their home ranges overlapped those of several females, and they visited one female after the other, probably for mating. So our study confirmed the results of other researchers: The striped mouse in the grasslands is solitary!

Social flexibility also 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 and resulting low population density in the Succulent Karoo would resemble the situation in grasslands and lead to a solitary mouse 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 males were no group members anymore, but visited one female after the other. Now after the drought, the home ranges of the mice increased significantly. They were much larger than in previous years in the same area of the Succulent Karoo. In fact, they were the same size as the home ranges of mice living in the grasslands. 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.

Future studies

The striped mouse shows extraordinary flexibility in its social system both between as well as within populations. Thus, it is an ideal model to study reasons for group living and social flexibility. In the future, our research will focus on following questions: 1. In how far is the social flexibility adaptive, i.e. leads to higher reproductive success? 2. How does a mouse determine which social strategy to follow, when to live in a group and when to live alone? 3. In how far is the social behaviour of a mouse influenced by the social environment it is growing up in? 4. What proximate mechanisms, especially endocrine factors, enable social flexibility? What hormones play a role? Thus, our main research focus is on the reasons of group living. Hereby we want to pay special attention to the role of males and understand under which (ultimate and proximate) conditions paternal care is shown.

Why research on the striped mouse?

There are many open questions, but the main question might be: Why do research on striped mice at all? 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 the influences of the environment on social behaviour and what physiological factors are associated with this. Humankind is exposed to an ever changing environment, mainly being changed by ourselves. Thus, we should be lucky to have an animal model that enables us to study the consequences - an animal that lives a few years, not decades, such that we can obtain the results in a relatively short time period.

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.

Mouse Portraits