sign in sign up
<<
Home , Ethology, Human ethology, Instinct, Konrad Lorenz, Nikolaas Tinbergen, Physiology

GENERAL ARTICLE The Careful

Sindhu Radhakrishna

What is it about the work of some great that sets them apart from the admirable work done by many good sci- entists? Is it because some, if not all, of their contributions stand the test of time? Or is it because their work paved the way for other great ideas to develop? Nikolaas Tinbergen’s and work suggests that it is a combination of both these factors that characterise a truly great scientist. Nikolaas Tinbergen (1907–1988) was a Dutch scientist who stud- ied behaviour. Tinbergen began his academic career at Sindhu Radhakrishna holds a master’s degree in the University of Leiden in the Netherlands and later moved to and a doctorate in animal , where he set up a school for animal behaviour stud- behaviour. She is presently ies. Tinbergen pioneered and popularised the of ethol- Professor and Dean at the ogy through his research and teaching. He lectured widely on Animal Behaviour and Programme, the subject and wrote extensively; some of his more well-known National Institute of books include The Study of (1951), The Herring Gull’s Advanced Studies, World (1953), Curious Naturalists (1958), and the Time-life vol- Bengaluru. Her research ume, Animal (1965). Tinbergen was an influential bi- interests are in the fields of , behavioral ologist within his lifetime and received many honours for his and conservation work, most notably, the , the Swammerdam Medal, , and her work is the Distinguished Scientific Contribution Award from the Ameri- focused on gaining a better can Psychological and the Diploma of Honour of the understanding of social behaviour and Sociedad Argentina Protectora de Animales. Apart from being in nocturnal an excellent communicator who mentored a new generation of . renowned , Tinbergen was also an exceptional photog- rapher and filmmaker who was celebrated for his films on animal behaviour.

Tinbergen is often described as one of the founding fathers of Keywords , or animal behaviour. This simplistic description, how- Animal behaviour, ethology, stick- ever, does not provide a holistic understanding of the importance leback fish, gull, stimuli, experi- ment.

RESONANCE | August 2018 845 GENERAL ARTICLE

Unlike early animal of Tinbergen’s achievements, and some historical context is nec- behavioural researchers essary to appreciate this. Animal behavioural science existed who relied on a long before Tinbergen began his work on animal behaviour; the ff approach and viewed crucial di erence being that the predominant approach then was behaviour as a one of comparative psychology, and psychologists largely viewed process, Tinbergen behaviour as a learning process. Tinbergen, on the other hand, believed that the answer was more interested in understanding why “ behave as to animal behaviour was in the hereditary they do?” and believed that the answer lay in the “hereditary influences occurring influences occurring inside the animal”. In other words, Tinber- inside the animal. gen saw behaviour as an evolutionarily adaptive trait and empha- sised a more objective, biological approach to understanding be- haviour. To understand why animals behave the way they do, Tinbergen observed animal behaviour in the of the and conducted painstakingly designed, simple field experiments to test out his hypotheses about how animals reacted to exter- nal stimuli. He studied a variety of species ranging from wasps and fish to gulls, blackbirds and kittiwake and showed how natural observation techniques can be married successfully to experiments within . Tinbergen’s field experiments were elegantly designed simple setups that carefully teased apart functional explanations for particular behaviours exhibited by an- imals and the of external stimuli that may elicit certain be- havioural responses from animals. The design of his earliest ex- periments on the orientation behaviour of the beewolf, Philanthus triangulum, highlighted what was to be the hallmark of his re- search – a careful, dogged approach that incrementally addressed the effect of one variable at a time, so that it was absolutely clear what kind of cues were being used by the beewolf females to ori- ent themselves (for a better idea about the design of Tinbergen’s beewolf experiments, please see Prof. Gadagkar’s article on ani- mal behaviour experiments in this issue). Tinbergen refined this research approach throughout his career. For example, when Tinbergen started studying the reproductive behaviour of the stickleback fish in the he set up at , he was initially interested in observing the

846 RESONANCE | August 2018 GENERAL ARTICLE behaviour of male and carefully docu- To prove that it was the mented the many steps in their . He noticed colour red that acted as that courting males turned red on their underside and attacked the ‘sign ’ or ‘releaser’, Tinbergen other coloured individuals that approached their territories. The designed a set of colour red appeared to be a stimulus that set off aggressive reac- experiments wherein he tions in the males, for male sticklebacks attacked the sides of the created some rough aquarium even when a red mail van passed beside the window of models of sticklebacks, painted them in various the aquarium. To prove that it was the colour red that acted as the colours, including red, ‘sign stimulus’ or ‘releaser’, Tinbergen designed a set of exper- and presented them to iments wherein he created some rough models of sticklebacks, the male sticklebacks in painted them in various colours, including red, and presented the tank. Red coloured models always elicited them to the male sticklebacks in the tank. Red coloured models more reaction from always elicited more reaction from courting males, demonstrat- courting males, ing that it was the colour red (rather than the shape/identity of demonstrating that it was the fish) that acted as the ‘releaser’ for a specific action from the the colour red (rather than the shape/identity of male. Tinbergen then continued with his experiments to show that the fish) that acted as the particular shape, size or type of movement can elicit certain ‘releaser’ for a specific reactions from males and females in the breeding period. For in- action from the male. stance, females will follow a red dummy fish and even try to move into a in the sand (where none exists), when the dummy fish is poked into the sand. Again, females will begin to lay eggs, when they are tapped repeatedly on the base of the tail (in a par- ody of the male prodding her tail base) although they observed the removal of the red fish that led them into the nest. These find- ings led Tinbergen to conclude that sticklebacks (and many other species) respond “simply to ‘sign stimuli’, i.e., to a few charac- teristics of an object rather than to the object as a whole....it is the signal, not the object, that counts. It seems to be typical of innate behaviour, and many social relationships in animals apparently are based on a system of signs.” Tinbergen’s careful experimentation (in natural conditions and in the laboratory) shows that he was an exceptional scientist, but it was his constant ability to learn that marks him as a truly out- standing . Tinbergen’s thinking about animal behaviour constantly evolved during the course of his research career and he built on the findings of his earlier studies to ask newer and more

RESONANCE | August 2018 847 GENERAL ARTICLE

exciting questions. For example, his earlier studies such as his work on Philanthus homing behaviour, and stickleback mating behaviour were built around the central question: What stimuli elicit innate and fixed behaviour patterns in animals? In his later studies, he moved on to ask: What is the of behaviour? His work on eggshell removal by the black-headed gull typifies this approach.

In a very curious Black-headed gulls remove eggshells from the vicinity of their behaviour, black-headed almost immediately after hatching. Except for the top end, gulls remove eggshells shells do not markedly differ from eggs. Yet, eggs are never re- from the vicinity of their nests almost moved from the nest. Tinbergen asked the question: What is immediately after the function of the eggshell removal behaviour? He hypothesised hatching. Except for the that it was to increase the survival chances of the chicks and pro- top end, shells do not ceeded to conduct a series of experiments to test out this hypoth- markedly differ from eggs. Yet, eggs are never esis. Tinbergen observed that the insides of the eggshells were removed from the nest. white which could attract the attention of predators. To build ev- idence for this point, he and his collaborators first conducted a set of three experiments wherein they investigated if the natural colour of the black-headed gulls’ eggs acted as camouflage and thereby protected them from the attention of predators. To do this, they painted some gull eggs white and left them alongside some unpainted eggs in shallow depressions in the ground that were similar to black-headed gulls’ nests. Comparative rates of preda- tion on the experimental eggs showed that the natural colour of the gulls’ eggs made them less vulnerable to than those painted white. Tinbergen then went on to test if the presence of the eggshells in the vicinity of nests increased chances of preda- tion. He did this by comparing the rates of predation on gull eggs that were placed near eggshells and those that were not. He also conducted another experiment wherein eggshells were placed at increasing distances from eggs to investigate the effect of prox- imity of eggshells on egg/chick predation. The results of his ex- periments conclusively proved that the presence of eggshells near eggs/chicks made them more vulnerable to predation and that the chances of predation decreased with increasing distance between eggs and eggshells.

848 RESONANCE | August 2018 GENERAL ARTICLE

The black-headed gull study demonstrates how Tinbergen could effectively deconstruct a simple animal behavior to show that ev- ery behavioral response has adaptive and evolutionary signifi- cance. In his discussion of this study, Tinbergen wrote: “Re- moval of an eggshell lasts a few seconds. It is normally done three times a year. Nothing would seem to be more trivial than this response, which at first glance might seem to be no more than fussy ‘tidying-up’ by a ‘house proud’ bird. Yet we have seen that it has considerable survival value and that the behavioural - isation is complicated and well adapted to the needs.”

Through his field experiments and emphasis on natural observa- Through his field tions, Tinbergen not only revealed several unexpected (and hith- experiments and erto unknown) aspects of animal behaviour, he also revolutionised emphasis on natural observations, Tinbergen the study of animal behaviour through this unusual approach. As not only revealed several described it, biologists “wear a white coat or unexpected (and hitherto Wellington boots, one or the other.....Tinbergen does both. In my unknown) aspects of book, that makes him the most important person in his field this animal behaviour, he also revolutionised the century.” study of animal Tinbergen is best remembered for his formulation of the ‘Four behaviour through this unusual approach. Questions of Ethology’. In his most famous paper ‘On Aims and Methods of Ethology’, published in 1963, he systematically laid out what he saw as the defining characteristics of ethology. This paper encapsulates his thinking (and changes in his views) about ethology over 30 years of his ethological career. To understand behaviour, he wrote, one must ask four main questions, namely: “(1) What is its physiological causation? (2) What is its func- tion or survival value? (3) How has it evolved over time?, and (4) How has it developed in the individual?” By “dividing be- haviour studies into , development, , and evolutionary history”, Tinbergen provided biologists with a clear and holistic framework for studying behaviour that would in later years be expanded to connect genes to behavioural phe- notypes. For this reason, Tinbergen’s four questions continue to remain as central to our understating of behaviour as they were when they were first published (see Prof. Gadagkar’s Article-in- a-Box on this classic paper in this issue). Although many early

RESONANCE | August 2018 849 GENERAL ARTICLE

Tinbergen’s four theories of ethology such as Lorenz’s psycho-hydraulic model questions about and Tinbergen’s hierarchical model of instinctive action have come behavioural causation, to be critiqued over the years, Tinbergen’s four questions about development, function, and still forms behavioural causation, development, function, and evolution still the cornerstone of forms the cornerstone of teachings in ethology. teachings in ethology. The hallmark of Tinbergen’s research contributions was his care- ful, patient observations and it was in this regard that he differed most significantly from his peer, collaborator and friend , one of the other founding fathers of ethology. Lorenz was a flamboyant personality, whose pronouncements on and took the biological world by storm, yet it is Tin- bergen’s methodology of careful experimentation and conceptual frameworks to study behaviour that has become the textbook ma- terial for all aspiring students of behaviour. , in his biographical sketch of Tinbergen, relates an incident that encap- sulates the differences in temperament and work between the two men. Post-World War II, Tinbergen and Lorenz met at a confer- ence in Cambridge in 1949. During one of their discussions, they talked about “how often you had to see an animal do something before you could say that the species did it. Konrad said he had never made such a claim unless he had seen the behaviour at least five times. Niko laughed and clapped him on the back and said “Don’t be silly, Konrad, you know you have often said it when you have only seen it once!” Konrad laughed even louder, ac- knowledging the point and enjoying the joke at his own expense.” Tinbergen’s contributions to biology are manifold. He advocated the biological approach to understanding behaviour that is taken for granted today, highlighted the importance of detailed, natu- ralistic observations in understanding behaviour, showed the pos- sibilities of designing simple field experiments that can answer questions related to the function and cause of a behaviour, and consistently stressed the need for careful studies that would build up evidence through careful observations and experiments to jus- tify any conclusions they made. Looking back, more than 50 years after the event, it is difficult to appreciate the difference that Tinbergen’s ideas have made to our understanding of animal

850 RESONANCE | August 2018 GENERAL ARTICLE and behaviour. Today behavioural ecology and evolution- ary are integral subdisciplines of biology and it is hard to imagine that Tinbergen’s work helped stimu- late the development of these fields. Tinbergen’s (and his col- leagues’) greatest accomplishment was that they made behaviour an integral part of biology, a ‘testable science’, and this particular achievement was due more to Tinbergen’s careful construction of how we can study behaviour than anything else. It is telling that in its history, the Nobel Prize has been given only once for animal behaviour. In his speech, granting the Prize to the trio of , Konrad Lorenz and Nikolaas Tinbergen, Borje¨ Cronholm talked about how the triumvirate had succeeded in transforming the study of behaviour to an analytical science, by treating be- haviour as a biological trait within an evolutionary framework. While von Frisch was awarded the prize for his work on honeybee communication and Lorenz for discovering fixed action patterns and imprinting, Tinbergen was cited for his ‘experimentation and the discovery of extra-normal stimuli that released cascades of actions’. Tinbergen passed away in 1988 in his home in Oxford after a long and fulfilling career in research and academics. Yet, every time biology students are introduced to the four questions of ethology or are taught about designing behavioural experiments, Tinbergen is reborn. And this, more than anything else, is why Nikolaas Tinbergen was a great scientist.

Suggested Reading Address for Correspondence Sindhu Radhakrishna [1] Roberts (ed), Special Issue on Tinbergen, Bulletin, 28, No 4, School of Natural 2013. and [2] Joan E Strassmann, Tribute to Tinbergen: The Place of Animal Behav- Room No: S 23 ior in Biology, Biology Faculty Publications and Presentations, Paper 43, National Institute of Advanced http://openscholarship.wustl.edu/bio_facpubs/43, 2014. Studies [3] N Tinbergen, On Aims and Methods of Ethology, Animal Biology, 55.4, pp.297– IISc Campus 321, 2005. Originally published in 1963. Bengaluru 560 012 [4] N Tinbergen, The Curious Behavior of the Stickleback, ScientificAmerican, India 187(6), pp.22–27, 1952. Email: [5] N Tinbergen, G J Broekhuysen, F Feekes, J C W Houghton, H Kruuk and sindhu.radhakrishna@ E Szulc, Eggshell Removal by the Black-headed Gull, Larus ridibundus L.,A gmail.com Behaviour Component of Camouflage, Behaviour, 19(1), pp.74–116, 1962.

RESONANCE | August 2018 851