November 14, 2013 by comparativelypsyched
It is a crisp autumnal morning, and I am pleasantly contemplative on this final leg of my commute. I have made this trip most mornings over the last three years yet traversing the steep slope gets no easier. With any distraction a respite, I stop to investigate the twittering from a nearby bush. It is not a rare bird- just a European robin (Erithacus rubecula)- but he is boldly and proudly singing his winter song. I pause to wonder: Why does the robin sing? And because sometimes the simplest questions require the most serious consideration, I take advantage of the nearest bench and think of a Dutch man who believed one question was not enough.
In 1963, Nikolaas Tinbergen dedicated the publication of a new paper to his good friend, Konrad Lorenz. In this article Tinbergen presented his case for a unified Ethology, the discipline he and Lorenz had cultivated, outlining one of his greatest contributions to the study of animal behaviour, his four questions. Sitting in the morning sun Tinbergen’s four questions help me explain the robin’s song.
Two of Tinbergen’s questions relate to proximate causation, i.e. the immediate causes of a behaviour. “How does this robin sing?”- in contrast to: “Why do robins sing?”- a question I will address shortly. One proximate question concerns the mechanism underlying a behaviour; the other enquires into ontogeny. I will first examine the mechanism of birdsong.
To examine the mechanism of a behaviour is to ask what events in the environment are necessary for a behaviour to occur and what processes lead to that behaviour. First of all, what in the environment caused this robin to sing? What are the necessary sensory inputs? The answer is rarely simple, but we can assume that the time of the day is important, as is the absence of a predator. Once the correct information is available, a variety of neurological computations will take place before the robin decides to sing. When these processes have occurred, air is forced through the robin’s vocal cords (or syrinx) creating vibrations in the air that I interpret as song.
But the robin wasn’t born knowing this melody. Questions of ontogeny ask what experience, or what learning, is necessary for a behaviour to develop. While most birds and other animals are born with an innate vocal repertoire, many songbirds must learn their songbook.
Researchers examining the development of birdsong have identified two stages of song-learning. In the sensory stage, a young bird, while listening to the song of a tutor, will create a mental template of that song. During the second stage, the sensorimotor phase, the bird practices singing, and by comparing their own song to the previously learned template, the bird gradually corrects their own melody until it matches the remembered version. Without the right experience, a young robin will never develop a complex song. For example, birds raised in isolation do not get to record a song’s template and will have nothing to compare their own song to when practising. If the robin I hear today was raised alone he would now be singing a different tune.
After considering proximate causation we can take a step back and study the ultimate causes of a behaviour. Questions of ultimate causation are concerned with the bigger evolutionary picture, asking when a behaviour evolved and why? To ask when a behaviour evolved is to enquire into phylogeny. When studying the evolution of an organ we can answer this question through an inspection of the fossil record. For example, if we were to ask at what point in the robin’s evolutionary past feathers evolved, we would examine the fossilised remains of the robin’s ancestors, pinpointing and dating the oldest specimen with feather-like structures. Using this method we know that the first birds descended from reptiles; indeed, the fossilised remains of an animal that marks an intermediate stage between reptile and bird has been discovered (see the famous archaeopteryx below).
Behaviour, however, leaves no fossilised trace so we must use alternative methods to infer an evolutionary history. A comparative approach requires an examination of the behaviours in groups of animals that are closely related. If the same behaviour is present throughout the range of related species we can assume the common ancestor of these species also performed the behaviour. If the robin sings, and the blackbird sings, and the reed warbler sings, we assume the common ancestor of these birds also sang. However, this method is not without problems, as a behaviour found in two species may also have evolved independently. For example, Nathan Emery and Nicola Clayton argue that the problem solving abilities demonstrated by corvids (crows, jackdaws, ravens, etc.) is very similar to the intelligent behaviours found in apes. In this case, it is highly unlikely that the common ancestor of chimpanzees and crows possessed these extraordinary mental abilities while they were subsequently lost in the non-ape/corvid lineages.
Convergent evolution, the independent evolution of a behaviour or trait, complicates the use of comparative methods, so when deciding whether a behaviour observed in two or more animals originated in a common ancestor or evolved independently a simple rule of thumb is used. Which explanation is the most parsimonious (i.e. the interpretation requiring the fewest logical steps). When a group of closely related individuals all share the same behaviour the most parsimonious explanation is to assume common inheritance; it is safe to assume that blackbirds and robins did not evolve song independently.
We can assume birdsong evolved millennia ago in some common ancestor of the songbirds we see every day (the Passeri clade). But why did birdsong evolve at all? Singing is costly, using up energy and advertising the singer’s location to predators. However, these costs must be outweighed by other benefits. The final question in Tinbergen’s toolbox addresses these benefits, a behaviour’s adaptive pay-off.
The robin’s song imparts many potential benefits. When it isn’t the breeding season the robin sings to advertise its territory, repelling intruders in the hope of preventing costly battles. If it was the breeding season, singing may serve to advertise some desirable quality of the singer. For example, male owls hoot less and have less elaborate hoots when they are carrying a greater number of parasites (Redpath et al. 2000). The robin’s song may play a similarly adaptive role.
These four questions can be applied to any of the robin’s many behaviours; indeed, these four questions can be applied to the behaviour we observe in any animal. Fifty years after the publication of his seminal paper, Tinbergen’s questions are still helping ethologists, comparative psychologists, and anyone with an interest in behaviour achieve a richer understanding of the animals they study. The answers keep changing, but the questions stay the same.
My robin does not remain on his perch for long and shortly I am left in the relative silence of a November morning. Renewing my commute I spot a herring gull land on nearby green verge. She rights herself, briefly preens and begins jogging in place. I pause for a moment to wonder about this odd display, but I soon walk on. I wonder, which would be a better avenue of study: Four questions for the jogging gull, or four questions for the procrastinating student.
Emery, N. J., & Clayton, N. S. (2004). The mentality of crows: convergent evolution of intelligence in corvids and apes. Science, 306(5703), 1903–7. (link)
Redpath, S. M., Appleby, B. M., & Petty, S. J. (2000). Do male hoots betray parasite loads in Tawny Owls ? Journal of Avian Biology, 31, 457–462.
Thorpe, W. (1954). The process of song-learning in the chaffinch as studied by means of the sound spectograph. Nature 173, 465–469.
Tinbergen, N. (1963). On aims and methods of ethology. Zeitschrift für Tierpsychologie, 20(4), 410–433. (link)