he/she is asking, and it could lead to futile arguments concerning whether the bird is singing to attract mates or because it learned its song. The same problem arises in all other areas of animal behavior, so it is very important to make clear which question is being addressed in any study. Of course, it is possible that a particular investigator wants to address more than one question at a time. This is perfectly legitimate, as long as it is made explicit which of the questions are addressed at what time. A famous example of this is an experimental paper by Tinbergen and his associates (Tinbergen et al. 1962) on the behavior of blackheaded gulls (Larus ridibundus). After the chicks have hatched, the adult birds remove the empty eggshells from the nest. Tinbergen and his students investigated both the causation and the function (survival value) of this behavior using elegantly designed simple field experiments. They discovered the stimulus characteristics of items removed from the nest and, in the same paper, also reported results relevant to nest predation.
There is also considerable overlap among the four questions. For instance, the development of behavior is essentially a causal problem but may also involve functional aspects (Chapter 7). The evolution of behavior often depends on mechanism. For instance, emergent properties of an animal’s sensory and perceptual capabilities (mechanisms) may create opportunities for sexual selection to operate in the evolution of extravagant traits (Chapters 12 and 14). Finally, questions in one domain (e.g., function) can provide clues for questions in another domain (e.g., causation). For instance, a number of bird species cache food, some for a few hours, others for months (Vander Wall 1990). It is plausible that the ecological circumstances that have given rise to these different forms of food caching may have also influenced the birds’ ability to memorize spatial locations. In fact, a large number of studies are concerned with investigating the spatial memory of food caching versus nonfood-caching birds (Chapter 8).
Trends in the Study of Animal Behavior
Behavioral ecology: from mechanism to function
Much of the research and theorizing of early ethologists such as Lorenz and Tinbergen was concerned with the causation of behavior. When Tinbergen was invited to move from the Dutch University of Leiden to the University of Oxford, he established the Animal Behaviour Research Group, while at the same time the ecological ornithologist David Lack was taking over the newly founded Edward Grey Institute of Ornithology. The coincidence of having both these scientists and their followers in the same department in Oxford sowed the seeds of a discipline that was to blossom much later in the mid-1970s under the name of behavioral ecology.
Behavioral ecology arose out of the fusion of evolutionary ecology, population ecology, and ethology. A number of conditions were ripe in the mid-seventies for such an event. In 1975 the Harvard entomologist Edward O. Wilson published Sociobiology, The New Synthesis (1975). Wilson’s book was firmly grounded in population genetics and evolutionary biology. Its clear presentation of William D. Hamilton’s concepts of inclusive fitness, kin selection, the evolution of altruism and social groups among others, provided the essential foundations for a successful evolutionary approach to social behavior. Not long after that, in 1978, John R. Krebs at Oxford University and Nicholas B. Davies at Cambridge co-edited a book they called Behavioural Ecology: An Evolutionary Approach, which applies a similar evolutionary approach but this time to all, not just social, behavior. The publication of that book marks the official birth of behavioral ecology, which now includes sociobiology (see Chapter 17).
Behavioral ecology today is more of an approach than a body of accumulated fact. Its initial success grew out of a combination of optimality theory and evolutionary thinking that pictures the expression of behavioral traits as constrained trade-offs between their evolutionary benefits and costs (Chapter 11). The development of the concept of the evolutionarily stable strategy (ESS) by the British evolutionary biologist John Maynard Smith (1982) allowed this cost–benefit approach to be applied to a wide range of behavioral interactions. Evolutionary thinking and the cost–benefit approach cast a new light on behavioral systems such as foraging, fighting, and habitat selection (Chapter 11). When applied to communication it raised an important number of questions concerning the design of signals and their functions (Chapter 14). While early ethologists tended to picture sexual reproduction as a cooperative venture between males and females, the evolutionary approach has somewhat subverted this idyllic view. Mating systems and mate choice (Chapter 12) as well as conflicts of interests between mates (Chapter 14) have become exciting and rapidly developing areas of the discipline. Darwin himself pictured behavior as a character that was modified over generations by selection. Behavior, hence, has a history that can be and is studied with contemporary organisms (Chapters 15 and 16).
Neuroethology and cognitive neuroscience
The mechanisms underlying behavior are also represented in the workings of the central nervous system. In fact, Tinbergen often used neural analogies and metaphors in his models of behavior. We shall see in Chapters 2 and 5 how the central nervous system obtains and processes information about its external world. As knowledge about the brain, both its gross and fine-level morphology as well as the way its neurons are connected, led to increased interface between brain and behavior a new subdiscipline arose that is called neuroethology (Ewert 1980; Chapter 2). In the early days of this new discipline, researchers concentrated on the study of the neural mechanisms of perception and movement, often in insects or simple vertebrates. More recently the study of the brain mechanisms of behavior is also directed at higher cognitive processes such as learning and memory or spatial orientation. Often, the terms behavioral neuroscience or cognitive neuroscience are used to describe these disciplines. Now, the combination of an extraordinary array of powerful techniques from electrophysiological recording to molecular analyses of RNA sequences allows researchers to delve deeper into the connection between behavior and its neural substrate (Chapters 5 and 9).
Cognitive ecology and neuroecology
Perhaps as a result of the success of behavioral ecology, the mechanisms of brain and cognition have also been studied more recently from a functional and/or an evolutionary perspective, in new fields known as cognitive ecology (Healy & Braithwaite 2000; Macphail & Bolhuis 2001) and neuroecology (Bolhuis & Macphail 2001). According to the former, an animal’s ability to collect and process information should be heavily influenced by its ecology. Neuroecology refers to the study of the neural mechanisms of behavior guided by functional and evolutionary principles. How do the evolutionary pressures for complex birdsong affect the evolution of the underlying neural substrate? How does having a large home range affect one’s ability to navigate? Does having to store food place selective pressure on spatial memory and its underlying brain regions? These functional and evolutionary approaches to the study of brain and cognition have come under considerable criticism from authors who claim that they are flawed, because Tinbergen’s four whys are being confounded (Bolhuis & Macphail 2001; Macphail & Bolhuis 2001; Bolhuis & Wynne 2009; Bolhuis 2015). For example,
