Behavior

When asking what is typically mammalian in behavior, we must first consider which adaptations and preconditions of a mammal normally shape its life and body. Mammals are warm-blooded, or endothermic, and their system of body temperature regulation through metabolism requires more energy than what is needed by ectotherms. Foraging is also an important aspect of behavior, and has to be considered as a decisive factor in shaping social systems. Also, mammals in general (and female mammals specifically) invest a lot more in terms of time, effort, energy, nutrition, and risk, into their offspring than most other vertebrates do. Again, this shapes social systems, in particular mating and rearing, but also puts severe demands on foraging strategies. Another characteristic is the highly developed brain, specifically in those areas that are necessary for behavioral plasticity and variability, such as the highly evolved forebrain and its hemispheres. This in turn allows the mammal to adapt to a diversity of ecological conditions, and also to form complex and individualized societies. In connection with the intensive and often long periods of infant care, not only by the parents but also other members of the group, this can lead, again, to highly variable and adaptable solutions to ecological as well as social problems and situations. In this chapter, we will cover two of those areas in which mammals are special: learning and behavioral plasticity, and social systems (which include mating and rearing as well as foraging and anti-predator systems). Each of these fields is currently the focus of scientific attention in many places, and by many different approaches. In order to fully understand any biological phenomenon, Tin-bergen in 1963 proposed to answer four questions, and only after getting satisfactory answers to all four can we presume that we have "explained" this phenomenon. They are:

Where did it come from in evolution?
What selective advantage does an individual get from having this particular trait (the so-called ultimate reasons)?
How does it work (physiology, so-called causal mechanisms)?
How does it develop in an individual's life (so-called ontogeny)?

We shall use these four questions to structure our discussion of mammalian behavior. In order to answer these questions, a combination of different scientific approaches is necessary. Thus, we will draw data from long-term field studies as well as from laboratory and zoo research, from experimental trials as well as from purely observational approaches, and will also need support from other biological disciplines such as endocrinology and molecular genetics. Behavior in itself is at the interface of genetics and ecology, and its under-standing is central also to questions of animal welfare, conservation biology, zoo management, and our relationship with pets and companion animals.

Behavioral plasticity

Learning in itself, of course, is by no means specific for mammals, or even higher animals. When asking the first Tin-bergen question, we then have to look for those areas of behavioral plasticity that distinguish mammals from their reptilian ancestors. So-called higher forms of learning, which require certain degrees of neural complexity, are (among others) spatial memory and cognitive mapping. Predators that follow prey, primate bands that follow certain routes between sleeping and foraging sites, caribou that migrate over long distances, and other mammals on the move often display an astonishing ability to cut corners, find shortcuts over ridges, circumvent deep parts in rivers after nightly rainfall, and still arrive at their destination without delay. Caribou that are delayed by late snowfall in spring even use these shortcuts to save time in migration. In all of these cases, some sort of "map" must be represented in the animals' nervous systems, and each element of the map must not only have an "address," but also a possibility to relate it to other elements. Another form of behavioral plasticity is called "problem-solving by insight." In typical cases, an animal is confronted by a situation it cannot immediately solve, such as bananas hanging too high to reach, or food hidden in a box. Problem-solving by insight requires that the animal first familiarize itself with the situation and then start to act in a goal-directed way (such as using a tool, elongating one stick with another one, or opening the lid of the box with a lever). Tool use has been described for mammals from at least six orders. A tool here is defined as a movable object that is not a fixed part of the animal's body, is being carried shortly before or during usage, and is positioned in an adequate way for its subsequent use. Following this definition, mongoose use tools to crack eggs, sea

otters carry stones as anvils, elephants use twigs to swat flies, primates throw stones and branches not only to defend themselves but also to detach fruit from trees, chimpanzees angle for termites, etc. Remarkably, more forms of tool use have been described from captive than free-ranging animals, and only in some apes do we have sufficient evidence for observational learning of tool use from the field.

Even though some of these higher forms of learning and cognition can be found in some birds as well, they are not yet in any case described from reptiles, and we can thus safely assume that the ability for them evolved somewhere in mammalian phylogeny. Thus, question number one seems at least partly answered.

What about selective advantage and survival value? It is of course easy to state that animals that learn better will be better able to cope with environmental challenges and will thus be more apt to survive. Hard evidence from carefully designed studies, however, is scarce. In several vole species of the genus Microtus, there is a clear correlation between spatial learning ability and ranging behavior: only in species where males have larger home ranges than females do males fare better in spatial learning (maze-running) tests. In food choice trials with rodents as well as ferrets and other carnivores, decision time was significantly shorter between novel, or new, foods for animals reared with a more variable diet. When an animal is quicker to reach a decision to eat something, it can eat more per given time, and the extra amount of nutrients certainly is an advantage. Feeding can also become more efficient when search-images have been developed, as demonstrated with hamsters and other rodents. Animals that learn about potentially dangerous predators, as ground squirrels do from hearing other colony members giving warning calls, are another example of learning with a direct survival value.

To address the third question, physiological correlates of learning are known for at least several learning phenomena: brain areas responsible for spatial learning are larger in males of those vole species whose spatial learning is better than females, but not in those without such a sex difference. The olfactory bulb in the brain of a young ferret during the critical period of olfactory food imprinting is larger than before or after this time. We also know that thyroxine, the hormone of the thyroid gland, is responsible for neurological changes during food imprinting in this species, and that oxytocin, a pituitary hormone, is necessary in the brain of monogamous animals to learn who their specific partner is during pair formation. Several areas in the limbic system of the brain, particularly the hippocampus, have been identified as being responsible for exploratory behavior and learning.

So, to address the fourth and last question, what data do we have about ontogenetic influences on behavioral plasticity?

When observing young mammals, play behavior is among the most obvious patterns performed regularly. There are many suggestions that during play, behavior is trained and general reactivity and adaptability is thus improved. Again, however, there are mostly plausibility arguments for this: "Because play occurs, and because it is costly in terms of time, energy, risk of injury, etc., it must have some positive effect. Otherwise, selection would have abolished it long since." Field studies of the same species under different conditions, with different amounts of juvenile play, often find less social cohesion in those individuals that played less. But this could also result from differences in other ecological conditions.

Nevertheless, we return to the question of learning and socialization in the discussion of social systems and social behavior. (There are, however, several studies on the influences of rearing condition and environmental factors on learning and problem-solving later in life.) From studies with laboratory rats and mice, we know, for example, that a well-structured environment, such as cages with climbing and hiding possibilities, is crucial to an animal's later ability to learn how to run through a maze, explore novel situations, climb over ropes, etc. The advantage of using laboratory rodents for these studies is that there are inbreeding strains that differ in learning ability. Thus we have "bright" and "dumb" mice, genetically speaking. However, rearing a "bright" mouse in a boring environment (standard lab cage) and a "dumb" mouse in an enriched, well-structured one leads to a near reversal of their genetic disposition—the "dumb" strain is now as good as, and

sometimes even better than, the "bright" one. Another approach to ontogenetic studies of learning and problem-solving was taken in studies with juvenile macaques and vervet monkeys. It was found that those monkeys who, as juveniles, were able to control their environment by deciding when to press a lever and get a food reward, later in life were more active in exploring and solving new situations that those that could press the same lever but received the same amount of food via random, computer-generated portions. Similar results are also described for domestic dog puppies raised in a challenging

Coyotes (Canis latrans) howl to defend their territory and inform others of their whereabouts. (Photo by Larry Allan. Bruce Coleman, Inc. Reproduced by permission.)

Social systems

The diversity of mammalian social systems

Sociality in the framework of Tinbergen's questions

Resources

Books

Periodicals

Behavior

Behavioral plasticity