Niko Tinbergen Research Articles

More sleep for behavioral ecologists.

From jellyfish to parrot fish and roundworms to homeotherms, all animals are thought to sleep. Despite its presumed universality, sleep is a poorly understood behavior, varying significantly in its expression across, and even within, animal lineages. There is still no consensus about the origin, architecture, ecology of sleep, or even its defining characters. The field of behavioral ecology has the potential to extend our knowledge of sleep behavior to nontraditional models and in ecologically relevant settings. Here, we highlight current efforts in diversifying the field to generate stronger synergies between historically human-focused sleep research and behavioral ecology. Our primary aim is for behavioral ecology to enhance sleep research by contributing crucial observations as well as by creating novel comparative and evolutionary frameworks. At the same time, sleep research can enhance behavioral ecology by exposing the relevance of sleep to wakeful behaviors. Nikolaas Tinbergen's four levels of analysis have served as a foundation for comprehensively addressing questions in behavior, and we introduce some Tinbergian approaches to examine the interplay between sleep and wake under ecologically meaningful conditions.

Sixty Years of Tinbergen’s Four Questions and Their Continued Relevance to Applied Behaviour and Welfare Research in Zoo Animals: A Commentary

Understanding animal behaviour can feel like deciphering a foreign language. In 1963, pioneering ethologist Nikolaas Tinbergen offered a key: four fundamental questions to dissect behaviour’s complexities and reduce interpretive bias. These “Four Questions” fall into two categories: Proximate (how?) and Ultimate (why?). The Proximate questions ask how the behaviour is triggered (Causation) and develops over time (Ontogeny). The Ultimate questions delve into its evolutionary history (Phylogeny) and purpose (Function). Traditionally used in behavioural ecology, Tinbergen’s framework finds new relevance in fields like sentience, welfare, conservation, and animal management. This paper illustrates how further integration of these Questions into applied research can improve outcomes. For example, captive animals can receive enrichment seemingly “unnatural” in origin and form. Does such enrichment trigger species-typical behaviours, fulfilling the same adaptive function as natural stimuli would? Understanding a species’ natural behaviour patterns and how the performance of such activities promotes positive welfare states is key to biologically relevant population management. Tinbergen’s Four Questions can help scientists to decipher the relevance of natural behaviour, and how a species’ responses to their environment indicate what individuals need and want at a specific time or place. By applying the Four Questions, we can answer this question and, in turn, refine husbandry practices and conserve behavioural diversity in managed populations. Sixty years after their conception, Tinbergen’s Four Questions remain a powerful tool for behavioural research. By embracing different biological disciplines within a unified framework, applied animal zoo science will continue to advance and provide credible evidence-based outputs.

A History of Biology

A History of Biology

50 years of the Nobel Prize to Lorenz, Tinbergen, and von Frisch: integrating behavioral function into an ethology for the 21st century

The 50th anniversary of the awarding of the Nobel Prize to Konrad Lorenz, Niko Tinbergen, and Karl von Frisch, arguably one of the most significant events in the history of ethology, has gone virtually unnoticed. Students and newcomers to the field may be wrongly led to believe that ethology has lost its prominent role as the leading discipline at the forefront of studies of animal behavior with a biological foundation. However, the decline of ethology is more apparent than real, in part a consequence of tying the discipline to a particular theoretical approach (i.e., that of classical ethology), but also due to the historical amnesia affecting many areas of science and the uneasy relationship of ethology with some of its own subdisciplines. Behavioral ecology emerged in the 1970s as an ethological subdiscipline devoted to the study of behavioral function, one of the four aims of ethology famously identified by Tinbergen. Behavioral ecology became extremely popular, but was criticized due to its narrow focus on behavioral function. With the new millennium came a return to a more balanced approach to the study of animal behavior, with frequent calls to recover the balance between the different areas of study and the integrative spirit that many consider one of the most distinctive features of ethology. Still, some behavioral ecologists contend that ethology disappeared shortly after Lorenz, Tinbergen, and von Frisch’s Nobel Prize award and has been replaced by behavioral ecology, and offer revisionist narratives of the aims and scope of both disciplines in support of this contention. Contrary to this view, modern ethology remains a necessary and coherent endeavor that encompasses and subsumes all four of Tinbergen’s aims, including those considered to be part of the agenda of behavioral ecology. The challenge for the next 50 years will be to preserve the ethological legacy of pursuing the four aims and their integration across levels of biological organization, taxa, methodologies, and interdisciplinary boundaries for a complete understanding of animal behavior.

Sudden bio-mathematical self-similarity and the uniqueness of human mass societies: from T-patterns and T-strings to T-societies.

With the explosive growth of human knowledge especially in the twenteeth century with even greater facilitation of access to knowledge, the world of even relatively recent great thinkers becomes daunting as seen from a modern viewpoint. Recently, humans ignored the existence of the complex intracellular world of cell organs, giant information molecules such as DNA, societies of specialized worker molecules (proteins), and generally the surprising nanoscale world visible to humanity since only a few decades ago. Moreover, computational power and video technology were inaccessible to all scientists from, for example, Aristotle to Freud, so new views and ideas seem to be expected about phenomena at all scales including nano and human. Some have arrived very recently. Thus urgently needed knowledge about the biology of animal and human behavior received the first Nobel Prize as late as 1973, in Physiology and Medicine, shared by Karl von Frisch, Konrad Lorenz, and Niko Tinbergen. Lorenz's Nobel lecture was entitled "Analogy as a Source of Knowledge" which did not mention self-analogy (self-similarity) as none of the species studied were part of others and knowledge of the nanoscale phenomena at the heart of this article had barely become available. The views and empirical findings presented in this article depend on such recent intracellular nanoscale insights and the development of a set of mathematical patterns, called T-system, of which only two are considered, the self-similar (i.e., parts having a structure similar to the whole) T-pattern and the derived T-string, a T-patterned material string (here, polymer or text). Specially developed algorithms implemented in the THEMETM software for T-pattern detection and analysis (TPA) allowed the detection of interaction T-patterns in humans, animals, and brain neuronal networks, showing self-similarity between animal interaction patterns and neuronal interaction patterns in their brains. TPA of DNA and text also showed unique self-similarity between modern human literate mass societies and the protein societies of their body cells, both with Giant Extra-Individual Purely Informational T-strings (GEIPIT; genomes or textomes) defining the behavioral potentials of their specialized citizens. This kind of society is here called T-society and only exists in humans and proteins, while the self-similarity between them only exists in human T-societies.

Lost: on what level should we aim to understand animal navigation?

Given that all interactions between an animal and its environment are mediated by movement, questions of how animals inherit, refine and execute trajectories through space are fundamental to our understanding of biology. As with any behavioural trait, navigation can be thought of on many conceptual levels - from the mechanistic to the functional, and from the static to the dynamic - as laid out by Niko Tinbergen in his four questions of animal behaviour. Here, we use a navigation-centric interpretation of Tinbergen's questions to summarise and critique advances in the field of animal navigation. We discuss the 'state of the art'; consider how a proximal/mechanistic understanding of navigation is not a prerequisite to understanding ultimate questions of evolutionary/adaptive importance; propose that certain aspects of animal navigation research - and certain taxa - are being neglected; and suggest that extreme experimental manipulations might lead to the mischaracterisation of non-adaptive 'spandrels' as functional navigational mechanisms. More generally, we highlight pressing questions within the field, the answers to which we believe are within reach, and highlight the important role that novel methods will have in helping us elucidate them.

Epistemological discipline in animal behavior studies: Konrad Lorenz and Daniel Lehrman on intuition and empathy.

Can empathy be a tool for obtaining scientific knowledge or is it incompatible with the detached objectivity that is often seen as the ideal in scientific inquiry? This paper examines the views of Austrian ethologist Konrad Lorenz and American comparative psychologist Daniel Lehrman on the role of intuition and empathy in the study of animal behavior. It situates those views within the larger project of establishing ethology as an objective science. Lehrman challenged Lorenz and Niko Tinbergen, the main founders of this field, to clarify their epistemological positions regarding how to deal with the subjectivity of the animals they studied as well as the scientist's own subjectivity. I argue that there was a tension between their desire to eliminate the subjectivities of ethological researchers (and of their subjects) and the public perception that Lorenz had a remarkable ability to enter into the lives of the animals he studied. I explain why Lorenz rejected empathy as valid in scientific inquiry, showing that his epistemological position was grounded in his ideal of science and his proposed ontology for ethology. Yet, Lehrman insisted that full detachment was neither possible nor desirable.

Beyond the InstinctDebate: Daniel Lehrman's Contributions to Animal Behavior Studies.

This paper examines the contributions of Daniel S. Lehrman (1919-1972) to animal behavior studies. Though widely cited as a critic of the early ethological program presented by Konrad Lorenz and Niko Tinbergen, other significant aspects of Lehrman's career and research have not received historical attention. In this paper, I offer a fuller account of Lehrman's work by situating his debate with ethologists within the larger context of Lehrman's early scholarly development under G. K. Noble and T. C. Schneirla, by examining his scientific research on the ring-dove as well as his epistemological views about the best way to understand animal behaviour, and by presenting his leadership in institution and network-building of interdisciplinary approaches to animal behavior. This essay highlights Lehrman's impact on the evolution of ethology, endocrinology, and developmental biology.

Nikolaas Tinbergen’s children’s bookKleew(1947): the story of a herring gull

In September 1942, the pioneering ethologist Nikolaas (Niko) Tinbergen (1907–1988), together with other intellectuals who had protested against the expulsion of Jewish academics from Leiden University, The Netherlands, by the invading Nazi forces, was incarcerated in Beekvliet hostage camp in North Brabant. In his weekly letters home Tinbergen wrote Klieuw, the serialized story of a herring gull ( Larus argentatus), based on his previous field work, for his three children. Another inmate in the camp, Louis (L. J. C.) Boucher, a publisher, encouraged Tinbergen to publish the story as a book. Tinbergen and his fellow prisoners were released in September 1944 and with academic life returning to normal, Tinbergen went on a three-month lecture tour to the United States in 1946. It was there that the book, translated into English, was first published in 1947 under the title Kleew. The Dutch edition titled appeared a year later and was more successful than the English version, with many adults and children reading and memorizing the book’s contents. Because of Tinbergen’s extraordinary clarity of expression, Klieuw was considered one of the best Dutch children’s books of its time.

Godman‐Salvin Prize

Godman‐Salvin Prize

The significance of building behavior in the evolution of animal architecture.

Animals make a diverse array of architectures including nests, bowers, roosts, traps, and tools. Much of the research into animal architecture has focused on the analysis of physical properties such as the dimensions and material of the architectures, rather than the behavior responsible for creating these architectures. However, the relationship between the architecture itself and the construction behavior that built it is not straightforward, and overlooking behavior risks obtaining an incomplete or even misleading picture of how animal architecture evolves. Here we review data about animal architectures broadly, with a particular focus on building by birds and social insects. We then highlight three ways in which a better understanding of building behavior could benefit the study of animal architecture: by clarifying how behavior leads to physical properties; by examining the costs and benefits of building behavior; and by determining the role of learning and how this interacts with selection on behavior. To integrate questions about building behavior alongside those about architectures, we propose a framework inspired by Niko Tinbergen's four questions, examining the mechanistic, ontogenetic, phylogenetic, and functional basis of animal building. By integrating the study of behavior and architecture across levels of analysis, we can gain a more holistic view of the behavior‐architecture interactions, and a better understanding of how behavior, cognition, and evolution interact to produce the diversity seen in animal architecture.

Leveling with Tinbergen: Four levels simplified to causes and consequences.

In 1963, Niko Tinbergen published his foundational manuscript identifying the four questions we ask in animal behavior-how does the behavior emerge across the lifespan (development); how does it work (mechanism); how and why did it evolve (evolution); and why is it adaptive (function). Tinbergen clarified that these 'levels of analysis' are complementary, not competing, thereby avoiding many fruitless scientific debates. However, the relationships among the four levels was never established. Here, we propose 'leveling' Tinbergen's questions to a single temporal timescale divided into causes (encompassing mechanism, development, and evolution) and consequences (encompassing function). Scientific advances now seamlessly link evolution, development, and mechanism into a continuum of 'causes'. The cause-consequence distinction separates the processes that precede (and lead to) a behavior, from the processes that come after (and result from) a behavior. Even for past behaviors, the functional outcomes are (historical) consequences of the causes that preceded them.

Karl von Frisch and the Discipline of Ethology.

In 1973, the discipline of ethology came into its own when three of its most prominent practitioners-Konrad Lorenz, Nikolaas Tinbergen, and Karl von Frisch-jointly received the Nobel Prize for Physiology or Medicine. Historians have shown how Lorenz and Tinbergen were central to the practical and theoretical innovations that came to define ethology as a distinct form of animal behavior research in the twentieth century. Frisch is rarely mentioned in such histories. In this paper, I ask, What is Frisch's relationship to the discipline of ethology? To answer that question, I examine Tinbergen's relationship to Frisch's grey card experiments between Tinbergen's time as a student at the University of Leiden in the mid 1920s and his 1951 publication of The Study of Instinct. In doing so, I highlight previously neglected affinities between Frisch's early career research and the program of classical ethology, and I show how Frisch's research meant different things at different times to Tinbergen and others working in the ethological tradition.

Een getekende kaart van De Beer

A drawn map of the island De Beer A century ago nature reserve De Beer was situated opposite Hoek van Holland. The young (and later famous) Niko Tinbergen wrote a book in 1930 about this ‘bird island’. His younger friend Jan Joost ter Pelkwijk made a kind of mental map of De Beer in 1932 with more than 80 sketches on it. This map is compared with the 1938 topographical map.

A Sexually Dimorphic Olfactory Neuron Mediates Fixed Action Transition during Courtship Ritual in Drosophila melanogaster.

Animals perform a series of actions in a fixed order during ritualistic innate behaviors. Although command neurons and sensory pathways responding to external stimuli that trigger these behaviors have been identified, how each action is induced in a fixed order in response to multimodal sensory stimuli remains unclear. Here, the sexually dimorphic lateral antennal lobe tract projection neuron 4 (lPN4) in male Drosophila melanogaster mediates the expression of a fixed behavioral action pattern at the beginning of the courtship ritual, in which a male taps a female body and then extends a wing unilaterally to produce a courtship song. We found that blocking the synaptic output of lPN4 caused an increase in the ratio of male flies that extended a wing unilaterally without tapping the female body, whereas excitation of lPN4 suppressed the transition from the tapping phase to the unilateral wing extension phase. Real-time calcium imaging showed that lPN4 is activated by a volatile pheromone, palmitoleic acid, whose responses were inhibited by simultaneous gustatory stimulation with female cuticular hydrocarbons, showing the existence of an "AND-gate" for multimodal sensory inputs during male courtship behaviors. These results suggest that the function of lPN4 is to suppress unilateral wing extension while responding to a female smell, which is released by appropriate contact chemosensory inputs received when tapping a female. As the female smell also promotes male courtship behaviors, the olfactory system is ready to simultaneously promote and suppress the progress of courtship actions while responding to a female smell.SIGNIFICANCE STATEMENT Although it has been 80 years since Konrad Lorenz and Niko Tinbergen introduced how multiple acts comprising separate innate behaviors are released in a fixed order according to external stimuli, the neural circuits responsible for such fixed action patterns remain largely unknown. The male courtship behavior of Drosophila melanogaster is a good model to investigate how such a fixed behavioral sequence is determined in the brain. Here, we show that lateral antennal lobe tract projection neuron 4 (lPN4) in D. melanogaster functions as an "AND-gate" for volatile and contact chemosensory inputs, mediating the expression of tapping behaviors before unilateral wing extension during male courtship rituals.

Methodological Signatures in Early Ethology: The Problem of Animal Subjectivity

What is the adequate terminology to talk about animal behaviour? Is terminology referring to mental or emotional states anthropomorphic and should therefore be prohibited or is it a necessary means to provide for an adequate description and should be encouraged? This question was vehemently discussed in the founding phase of Ethology as a scientific discipline and still is. This multi-layered problem can be grasped by using the concept of methodological signatures, developed by Köchy et al. (2016c). It is designed to analyse and systematically compare animal research approaches by examining their common parameters. By examining the works of Konrad Lorenz (1903–1989) and Nikolaas Tinbergen (1907–1988), this paper offers new insights both on a methodological and theoretical level. Methodologically, the application of the concept of methodological signatures is illustrated; theoretically, the principles of Classic Ethology are analysed. My aim is to illustrate how the problem of scientific access to animal subjectivity was addressed in the history of Ethology by analysing statements about animal sentience. For this purpose, I will first outline the general discussion about animal subjectivity and the tension between anthropomorphism and empirical adequacy. I introduce my own theoretical and methodological framework before presenting an analysis of Lorenz’ and Tinbergen’s methodological signatures. Thereby, I show how the question of terminology is deeply embedded in a network of epistemological, methodological and ontological concepts and establish key characteristics in regard to ethological approaches to animal subjectivity. Finally, I shed light on the possibility of using this typology to examine current frameworks of animal welfare research.

An ethologic approach to differential diagnosis of autism in toddlers

Almost 50 years ago, ethology was involved in the diagnosis and treatment of autism through Niko Tinbergen, who had been studying it in the late seventies and early eighties, a period when knowledge of neurodevelopmental disorders, including autism, was just beginning. Decades later, in present times, when a number of informations are available on what has been the itinerary of the concept of autism and its concrete consequences in various parts of the world as well as on new data collected on this topic and other neurodevelopmental disorders, it may be useful to renew a study of these subjects in order to evaluate the positive role of ethology in the differential diagnosis and treatment of these conditions.

Hunters and Gatherers of Pictures: Why Photography Has Become a Human Universal.

Photography is ubiquitous worldwide. We analyzed why people take, share, and use personal photographs, independent of their specific cultural background. These behaviors are still poorly understood. Experimental research on them is scarce. Smartphone technology and social media have pushed the success of photography, but cannot explain it, as not all smartphone features are widely used just because they are available. We analyzed properties of human nature that have made taking and using photographs functional behaviors. We did this based on the four levels, which Nikolaas Tinbergen suggested for analyzing why animals behave in a particular way. Including findings from multiple disciplines, we developed a novel conceptual framework—the “Mental Utilization Hypothesis of Photography.” It suggests that people adopt photography because it matches with core human mental mechanisms mainly from the social domain, and people use photography as a cognitive, primarily social coping strategy. Our framework comprises a range of testable predictions, provides a new theoretical basis for future empirical investigations into photography, and has practical implications. We conclude that photography has become a human universal, which is based on context-sensitive mental predispositions and differentiates itself in the social and societal environment.

Nothing in Cognitive Neuroscience Makes Sense Except in the Light of Evolution

Evolutionary theory should be a fundamental guide for neuroscientists. This would seem a trivial statement, but I believe that taking it seriously is more complicated than it appears to be, as I argue in this article. Elsewhere, I proposed the notion of “bounded functionality” As a way to describe the constraints that should be considered when trying to understand the evolution of the brain. There are two bounded-functionality constraints that are essential to any evolution-minded approach to cognitive neuroscience. The first constraint, the bricoleur constraint, describes the evolutionary pressure for any adaptive solution to re-use any relevant resources available to the system before the selection situation appeared. The second constraint, the satisficing constraint, describes the fact that a trait only needs to behave more advantageously than its competitors in order to be selected. In this paper I describe how bounded-functionality can inform an evolutionary-minded approach to cognitive neuroscience. In order to do so, I resort to Nikolaas Tinbergen’s four questions about how to understand behavior, namely: function, causation, development and evolution. The bottom line of assuming Tinbergen’s questions is that any approach to cognitive neuroscience is intrinsically tentative, slow, and messy.

David W. Schindler—Icon and Iconoclast

David W. Schindler—Icon and Iconoclast