What is the behaviour?


Although the concept of behaviour may seem so trivial that does not even require to be defined, the reality is that there is surprisingly quite wide speared disagreement on what actually qualifies as behaviour in a biological context. One of the interpretation is that behaviour is the internally coordinated responses (actions or inactions) of whole living organisms (individuals or groups) to internal and/or external stimuli, excluding responses more easily understood as developmental changes (Levitis et al. 2009).

Animal behaviour refers to what animals do. Human fascination with animal behaviour probably extends back millions of years. Initially, animals were probably observed for practical reasons because early human survival depended on knowledge of animal behaviour. Whether hunting wild game, keeping domesticated animals, or escaping an attacking predator, success required intimate knowledge of an animals behaviour. Even today, information about animal behaviour is of considerable importance (www.britannica.com). For example, investigations of the foraging of insects pollinators, such as honeybees and bumblebees, have led to impressive increases in tomato yields throughout the world (Cooley and Vallejo-Marín 2021).

Figure: Effect of pollination treatment on percent change in tomato fruit weight compared to a no-pollination control across 71 experiments from 24 studies. Open pollination (n = 12), buzzing bee (n = 35), mechanical vibration (n = 13), non-buzzing bee (n = 6), auxin (n = 5). From Cooley and Vallejo-Marín (2021).

The origins of the scientific study of animal behaviour lie in the works of various European thinkers of the 17th to 19th centuries. Here, enough to mention Charles Darwin, whose publication On the Origin of Species (1859) has greatly shaped the way we look at animal behaviour. Since then animal behaviour is considered a trait which as any other trait evolves, being under various selective pressures (behavioural ecology) and affecting animal fitness (evolutionary ecology). Various aspects of animal behaviour can be considered (ethology), and only multidisciplinary approach allows to properly examine animal behaviour.

How to study animal behaviour?

Let’s start quite unusually, with a joke :)

Sherlock Holmes and Dr Watson went on a camping trip. After a good meal and a bottle of wine they lay down for the night, and went to sleep. Some hours later, Holmes awoke and nudged his faithful friend.
Holmes: “Watson, look up at the sky and tell me what you see.”
Watson: “I see millions and millions of stars.”
Holmes: “What does that tell you?”
Watson (pondered for a minute): “Astronomically, it tells me that there are millions of galaxies and potentially billions of planets. Astrologically, I observe that Saturn is in Leo. Horologically, I deduce that the time is approximately a quarter past three. Theologically, I can see that God is all powerful and that we are small and insignificant. Meteorologically, I supect that we will have a beautiful day tomorrow. Why, what does it tell you?”
Holmes (silent for a minute): “Watson, you are imbecile. A bastard has stolen our tent.”


Not being constraint with anything, Watson let his imagination run wild and considers the situation in different context. Studying animal behaviour is a bit like “watsoning”. To fully understand the behaviour, it is important to consider it from multiple perspectives. For that, one needs to ask various questions.

When we look/listening to at a singing of the robin, we can ask:

  • At what time of day does the robin sing?
  • Which organs and physiological processes are involved in (robin’s) singing?
  • Do all robins sing in the same way?
  • What purpose does this (robin’s) singing serve?
  • Do evolutionary ancestors or other close relatives of the robin sing similarly?
  • Etc…. (curiosity and imagination set the limit! :)


All these questions are interesting, and all they are valid. They all need to be answered to understand how and why the robin sings. The only thing is that you need to make your question/s very clear to get a clear answer/s. Insight of Niko Tinbergen, one of the founders of modern ethology, helped a lot in clarifying these questions. In his seminal paper ‘On aims and methods of ethology’, where he first outlined the four ‘major problems of biology’, he proposes classification of the questions on animal behaviour.

Four Tinbergen’s questions

  1. Function (or adaption): Why is the animal performing the behaviour? In which way does the behaviour increase the animal’s fitness (i.e. its survival and reproduction)?

  1. Evolution (or phylogeny): How did the behaviour evolve? How has natural selection modified the behaviour over evolutionary time? This is typically addressed by the comparative approach, where the behaviour in question is compared among closely related species.

  1. Causation (or mechanism): What causes the behaviour to be performed? Which stimuli elicit or what physiological mechanisms cause the behaviour?

  1. Development (or ontogeny): How has the behaviour developed during the lifetime of the individual? In what way has it been influenced by experience and learning?

The four types of questions operate at two different levels. Questions 1 and 2 give ultimate or evolutionary explanations. These are answers that take a longer perspective and try to explain why the behaviour has evolved. On the other hand, questions 3 and 4 give proximate explanations. These are answers that look into the immediate mechanical reasons for why a behaviour is expressed. To obtain a full understanding of the costs, benefits and constraints that have shaped a given behaviour both ultimate and proximate answers must be obtained.

Only examining animal behaviour and through the perspective of the these questions and at various levels one can truly understand the issue, and fill up the gaps in knowledge, like in a periodic table:


Niko Tinbergen biogram note (from royalsociety): Dutch-born Nikolaas (Niko) Tinbergen grew from a boy who loved skipping school to be outdoors, into a Nobel Prize-winning founding father of ethology – the science of animal behaviour. In the prime of his career, Niko’s energy and rigour outweighed his worsening depression, to produce many influential contributions to the field. In a short autobiography, Niko summed up his life: “I have been…rather like a butterfly flitting cheerfully from one flower to the next, rather than like a steadily working, “flower-constant” worker honey bee. But such has always been my nature, and if…as a consequence [I] have both missed much and gained much, I have at least been true to my nature.”


Birds (robin) singing is one of few study systems that have been truly considered through the perspective of all the four questions (Bateson and Laland 2013).

(A) Mechanism. Now we have pretty good understanding of the mechanisms underlying bird-song learning and production, central to which is ‘the song system’, a well-mapped neural circuitry of brain nuclei and their projections within the songbird brain.
(B) Function. Birds sing primarily to advertise their quality, with songs functioning as signals both to warn off rivals and attract mates.
(C) Development. Experimental investigations, such as rearing nestlings in captivity isolated from adults, have revealed that songbirds typically learn their songs early in life. The song is learned during a sensitive period, when birds are predisposed to learn the songs of conspecifics. The image shows sonograms of a typical wild chaffinch song and of the song of a chaffinch reared in isolation.
(D) Evolution. Comparative analyses have established that song features vary along phylogenetic lines, such clicks in the songs of orioles.

Figure: Tinbergen’s four questions in one system. From Bateson and Laland (2013).


The four Tinbergen’s questions are still valid, additional questions can be now added, such as: ‘How is the behaviour inherited?’, ‘What is the character?’, and ‘Of what is an animal seemingly aware?’. (Bateson and Laland 2013).

Methodology

Given a great variety of systems/species/topics, it is simply impossible to present the whole methodology that could be applied for studying animal behaviour. One of the most important issue, however, is the difference between observational and experimental studies. Both approach are useful, both have their pros and cons but the most common misunderstanding is the interpretation of correlation revealed in am observational study. It happens that a trend between two continous variables in an observational studies is interpretted as a causation, which is wrong!! Only in an experimental setting one can be sure (and so interpret) that a correlation means causation.

A funny stork example:

Modern technology helps a lot - for example avian migration

For a very long time animal behaviour was measured (whatever the setting – observational or experimental) simply by observing individuals (i.e. a human observer watched and noted what had spotted). This approach has a lot of advantages (cheap, often quite efficient or at least enough efficient for given question) but it is not free of constraints. Apart from that that human eye may not be able to register all details of given behaviour, it may also be prone to simple human errors and biases. Modern technology applied in animal behaviour not only improves accuracy and reliability of data we collect but sometimes simply reveal aspects of the behaviour we would never be able to discover with a bare eye.

Birds migration is a great example here. The first knowledge about avian migration patterns we have, comes from recoveries of ringed individuals (of course, one could develop these story here but for the purpose of the present topic it does not really matter, and generally speaking, it is how this all has started). For that birds were massively ringed in one site, to be recaptured somewhere else. Obviously, this recapture rate very much depends on species (size/behaviour/ecology) and research activity but overall it is very small. For instance, of 10000 ringed individuals of small passerine species one can/could count on few recaptures. But even from that we have learnt a lot, not only about pathways but also wintering areas of migrating species, etc. Based on that we could develop various hypotheses on birds behaviour during migration. To verify them, however, ringing is not reliable/efficient methodology and we need to go for technology achievements. GPS and/or GLS that we can deploy on birds (electronic devices that can register geographic location of the tagged individual in a given time) are of big advantage here. Still there are lot of constraints of the available equipment but technology keeps developing so we are still having lot to examine in the matter.

Modern technology helps a lot – measuring (un)measurable


Sometimes using modern technology allows to discover what we have not even expected to exist. A great (my favourite) example of that is a behaviour of the blue-capped cordon-bleu (Uraegintus cyanocephalus). Here, a slow-motion recording was applied so one could say that technology in not really a racket science but using this “simple” settings the allowed to reveal tap dancing of breeding partners. This dancing behaviour has long been recognized as a mating/courtship behaviour but nobody really knew that it is so much complex! See, how it looks like red-chicked cordon bleu


From Ota et al (2013)

Antropomorphism

Antropomorphism is attributing human traits, emotions, intentions to non-human entities (in ethology, animals). Looking at these polar bears and dogs in an anthropomorphic way, we could say bears want to play with dogs. Where is anthropomorphism? Well, in italics. We say that based on our way we interact in a social environment but what bears want, and is it a play it may not be that obvious.

Antropomorphism is a inherited trait of human being. There is some recognition on driving forces behind anthropomorphism, and as a matter of fact there is a marked increase in interest in the concept of anthropomorphism (e.g. Urquisa-Haas and Kortschal 2015) but regardless of the mechanisms behind its consequences for animal welfare, conservation and even as a potential constraint in animal behaviour research are important issue (Butterfield et al 2012).

Literature cited

Bateson P, Laland KN (2013) Tinbergen’s four questions: An appreciation and an update. Trends Ecol Evol 28:712–718. doi: 10.1016/j.tree.2013.09.013

Butterfield ME, Hill SE, Lord CG (2012) Mangy mutt or furry friend? Anthropomorphism promotes animal welfare. J Exp Soc Psychol 48:957–960. doi: 10.1016/j.jesp.2012.02.010

Cooley H, Vallejo-Marín M (2021) Buzz-pollinated crops: A global review and meta-analysis of the of supplemental bee pollination in tomato. J Econ Entomol 114:505–519. doi: 10.1093/jee/toab009

Höfer T, Przyrembel H, Verleger S (2004) New evidence for the Theory of the Stork. Paediatr Perinat Epidemiol 18:88–92. doi: 10.1111/j.1365-3016.2003.00534.x

Levitis DA, Lidicker WZ, Freund G (2009) Behavioural biologists do not agree on what constitutes behaviour. Anim Behav 78:103–110. doi: 10.1016/j.anbehav.2009.03.018

Ota N, Gahr M, Soma M (2015) Tap dancing birds: the multimodal mutual courtship display of males and females in a socially monogamous songbird. Sci Rep 5:16614. doi: 10.1038/srep16614

Urquiza-Haas EG, Kotrschal K (2015) The mind behind anthropomorphic thinking: Attribution of mental states to other species. Anim Behav 109:167–176. doi: 10.1016/j.anbehav.2015.08.011