Tribute to Tinbergen: Putting Niko Tinbergen's ‘Four Questions’ in Historical Context

Niko Tinbergen's (Zeit. Tier. 20, 1963, 410) paper ‘On aims and methods of ethology’ is appropriately remembered as the paper in which Tinbergen characterized ethology as ‘the biological study of behavior’ and went on to explain that to study behavior biologically is to ask four distinct questions about it: (1) How is it caused physiologically? (2) What is its survival value? (3) How has it evolved? and (4) How does it develop in the individual? Here, we consider Tinbergen's paper in its historical context by looking at it from three different perspectives: (1) a comparison of Tinbergen's formulation of ‘ethology's four questions’ with similar, but different formulations of biology's basic problems offered by Julian Huxley, Konrad Lorenz, and Ernst Mayr; (2) a survey of the roles that the four questions played in Tinbergen's own work over the course of his career; and (3) a consideration of the two explicit goals of Tinbergen's (Zeit. Tier., 20, 1963, 410) paper, namely (a.) to honor Tinbergen's friend and colleague Konrad Lorenz (as part of a Festschrift for Lorenz on the occasion of his sixtieth birthday) and (b.) to provide a sketch of ethology's scope and an evaluation of the ways the field needed to develop in the future. We suggest that just as the work of Tinbergen's Oxford research team revealed how the behavior of gulls reflected compromises worked out in the face of the diverse selective pressures of particular environments, we can identify certain conflicts that arose for Tinbergen in trying to write something that his friend Lorenz would like while also assessing ethology's current state and future prospects. That said, however, Tinbergen's enduring concern was to do all he could to ensure that ethology thrive as a field and develop a scientific understanding of animal (and human) behavior. For this to happen, he insisted, the four questions of ethology needed to be pursued in a balanced, comprehensive, and integrated fashion.     

History of developmental neuroethology: early contributions from ethology.

Ethology has its roots in the natural history of animal behavior. Questions of causation and function have historically been complementary, and each has rested upon a prior appreciation of the behavior of animals in nature. It is thus difficult to place a single time or place where ethology was born. Early evolutionary interests hinted at developmental constraints that continue to guide much research. It has only been relatively recently, however, that the explicit analysis of neural mechanisms in behavior has received the attention it deserves in developmental analyses. A mature developmental neuroethology will require a synthesis of the broad insights of ethology with refined neurobiological technique. Fundamental, however, is the primary focus upon behavior as it normally occurs.     

History of developmental neuroethology: Early contributions from ethology

Ethology has its roots in the natural history of animal behavior. Questions of causation and function have historically been complementary, and each has rested upon a prior appreciation of the behavior of animals in nature. It is thus difficult to place a single time or place where ethology was born. Early evolutionary interests hinted at developmental constraints that continue to guide much research. It has only been relatively recently, however, that the explicit analysis of neural mechanisms in behavior has received the attention it deserves in developmental analyses. A mature developmental neuroethology will require a synthesis of the broad insights of ethology with refined neurobiological technique. Fundamental, however, is the primary focus upon behavior as it normally occurs. © 1992 John Wiley & Sons, Inc.     

Are Animals Just Noisy Machines?: Louis Boutan and the Co-invention of Animal and Child Psychology in the French Third Republic

Historians of science have only just begun to sample the wealth of different approaches to the study of animal behavior undertaken in the twentieth century. To date, more attention has been given to Lorenzian ethology and American behaviorism than to other work and traditions, but different approaches are equally worthy of the historian’s attention, reflecting not only the broader range of questions that could be asked about animal behavior and the “animal mind” but also the different contexts in which these questions were important. One such approach is that represented by the work of the French zoologist Louis Boutan (1859–1934). This paper explores the intellectual and cultural history of Boutan’s work on animal language and the animal mind, and contextualizes the place of animal behavior studies within late-nineteenth-and early-twentieth-century French biology. I explore the ways in which Boutan addressed the philosophical issue of whether language was necessary for abstract thought and show how he shifted from the idea that animals were endowed with a purely affective language to the notion that of they were capable of “rudimentary” reasoning. I argue that the scientific and broader socio-cultural contexts in which Boutan operated played a role in this transition. Then I show how Boutan’s linguistic and psychological experiments with a gibbon and children provide insights into his conception of “naturalness.” Although Boutan reared his gibbon at home and studied it in the controlled environment of his laboratory, he continued to identify its behavior as “natural.” I specifically demonstrate the importance of the milieu of the French Third Republic in shaping Boutan’s understanding not only of animal intelligence and child education, but also his definition of nature. Finally, I argue that Boutan’s studies on the primate mind provide us with a lens through which we can examine the co-invention of animal and child psychology in early-twentieth-century France.     

What Capabilities for the Animal?

In this essay, I defend a bi-constructivist approach to ethology—a constructivist ethology assuming that each animal adopts constructivist strategies. I put it in opposition to what I call a realist-Cartesian approach, which is currently the dominant approach to ethology and comparative psychology. The starting point of the bi-constructivist approach can be formulated as a shift from the classical Aristotelian question “What is an animal?” to the Spinozean question, which is much less classical but which seems to me to be much stronger: “What are the capacities of the animal?”. Is it possible to conceptualize an ethology which insists on interpretation and therefore on invention, innovation and creativity, rather than on causality, the monotony of behavioural routines, and/or genetic or environmental determination? Such an ethology would be based not on the fiction of an absent observer but on fully recognizing the necessity of an observer, who is effectively present in order to get an observation. A pluralistic ethology does not dissociate itself from the marginal epistemologies of practitioners like animal trainers, hunters, stockbreeders etc., or, moreover, non-western experts. An ethology of this kind is not clamped within the boundaries of purely academic epistemology, obsessed by demarcation lines between the human and the animal. My work on the bi-constructivist approach represents a contribution towards the elaboration of an authentically biosemiotic ethology, one which is significantly different from the mechanical ethology of today.     

Fixing Content and Function in Neurobiological Systems: The Neuroethology of Electroreception

Are attributions of content and function determinate, or is there no fact of the matter to be fixed? Daniel Dennett has argued in favor of indeterminacy and concludes that, in practice, content and function cannot be fixed. The discovery of an electrical modality in vertebrates offers one concrete instance where attributions of function and content are supported by a strong scientific consensus. A century ago, electroreception was unimagined, whereas today it is widely believed that many species of bony fish, amphibians, sharks, skates, and rays possess this non-human sensory modality. A look at the history of science related to this discovery reveals a highly interdisciplinary endeavor, encompassing ethology, behavioral analysis, neuroscience, and evolutionary biology. While each area provides important evidence, none is sufficient on its own to fix content and function. Instead, I argue that an interdisciplinary, neuroethological approach is required to carry out such determinations. Further, a detailed consideration of biological research suggests that while content and function claims are empirically underdetermined and uncertain, there is insufficient reason to believe in an additional problem of indeterminism. In particular, Dennett's indeterminism arises from a research methodology -- logical adaptationism -- that generates evidence from only one of the areas of neuroethology. However, logical adaptationism does not reflect adaptationism as it is practiced in contemporary biology. I conclude that Dennett is faced with a dilemma: On the one hand, he can hold to logical adaptationism and the indeterminism that results from it, while giving up the relevance of his arguments to biological practice. On the other, he can embrace a more accurate version of adaptationism -- one which plays a role in a larger neuroethological framework -- but from which no strong indeterminacy claims follow.     

Tribute to Tinbergen: The Place of Animal Behavior in Biology

Tinbergen is famous for emphasizing behavioral fieldwork and experimentation under natural circumstances, for founding the field of ethology, for getting a Nobel Prize, and for mentoring Richard Dawkins. He is known for dividing behavior studies into physiology, development, natural selection, and evolutionary history. In the decades since Tinbergen was active, some of the best research in animal behavior fuses Tinbergen's questions, connecting genes to behavioral phenotypes, for example. Behavior is the most synthetic of the life sciences, because observing the actions of an organism can tell us what all those physical and physiological traits are for. Insights from behavior tell us how traits in one individual impact those in another in ways that challenge our definition of an organism. Behavioral conflict and cooperation among animals has led to theory that explains within‐organism conflict and cooperation and human malfunctions of many kinds. Darwin certainly began the evolutionary study of behavior, but Tinbergen brought it forward to the heart of biology. The challenge for the future is to apply concepts from animal behavior across biology with tools that would have amazed Tinbergen.     

The Ethological Approach to the Study of Human Behavior

Human ethology, which was established on the basis of classical zooethology, can be an inspirational contribution to the study of human behavior. The study of behavior in natural conditions is stimulating as well as the primary interest of ethologists in such behavioral patterns showing evolutionary success and benefits and which are called inborn or innate. The extensive area of human behavior, nonverbal communication, can be investigated also with the application of some ethological knowledge. Human ethology can bring significant insight to the evaluation of the pathology of human behavior in various medical disciplines. An important task of medical prediction (prognosis) can be made more reliable by considering the ethology. A specific attribute of the species Homo sapiens, his culture, is acknowledged and discussed through human ethology.     

Behavioural ecology's ethological roots

Since Krebs and Davies's (1978) landmark publication, it is acknowledged that behavioural ecology owes much to the ethological tradition in the study of animal behaviour. Although this assumption seems to be right-many of the first behavioural ecologists were trained in departments where ethology developed and matured-it still to be properly assessed. In this paper, I undertake to identify the approaches used by ethologists that contributed to behavioural ecology's constitution as a field of inquiry. It is my contention that the current practices in behavioural biology owe ethology something much subtler than the simple transposition of Tinbergen's Four Problems for heuristic purposes. Demonstrating what ethology inherited from the long naturalist tradition shows the tensions that strained the field and that later led to the loss of both its unity and its specificity. It also allows for a precise delineating of what behavioural ecology picked up from the ethological practice, and it helps to cast some light on the introduction of economical thinking in behavioural sciences.     

Culture and Pathology: Flathead Loneliness Revisited

My earlier considerations of Flathead loneliness and depressive disorder yielded an interpretation that emphasized the lack of necessary pathology in the Flathead experience of loneliness. In this paper I detail a shift in my thinking about the pathological character of loneliness, a shift traceable to a set of interactions that have led me away from illness experience and diagnosis to questions of treatment, intervention, and healing. I explore how this new set of questions refocused my attention-away from an exclusive preoccupation with the lonesome individual. I conclude with a reimagination of the pathological dimensions of Flathead loneliness as aspects of both group and individual health.     

Why Was Thomas A. Sebeok Not a Cognitive Ethologist? From “Animal Mind” to “Semiotic Self”

In the current debates about zoosemiotics its relations with the neighbouring disciplines are a relevant topic. The present article aims to analyse the complex relations between zoosemiotics and cognitive ethology with special attention to their establishers: Thomas A. Sebeok and Donald R. Griffin. It is argued that zoosemiotics and cognitive ethology have common roots in comparative studies of animal communication in the early 1960s. For supporting this claim Sebeok’s works are analysed, the classical and philosophical periods of his zoosemiotic views are distinguished and the changing relations between zoosemiotics and cognitive ethology are described. The animal language controversy can be interpreted as the explicit point of divergence of the two paradigms, which, however, is a mere symptom of a deeper cleavage. The analysis brings out later critical differences between Sebeok’s and Griffin’s views on animal cognition and language. This disagreement has been the main reason for the critical reception and later neglect of Sebeok’s works in cognitive ethology. Sebeok’s position in this debate remains, however, paradigmatic, i.e. it proceeds from understanding of the contextualisation of semiotic processes that do not allow treating the animal mind as a distinct entity. As a peculiar parallel to Griffin’s metaphor of “animal mind”, Sebeok develops his understanding of “semiotic self” as a layered structure, characterised by an ability to make distinctions, foremost between itself and the surrounding environment. It appears that the history of zoosemiotics has two layers: in addition to the chronological history starting in 1963, when Sebeok proposed a name for the field, zoosemiotics is also philosophically rooted in Peircean semiotics and German biological philosophy. It is argued that the confrontation between zoosemiotics and cognitive ethology is related to different epistemological approaches and at least partly induced by underlying philosophical traditions.     

A biological approach to computational models of proteomic networks

Computational modeling is useful as a means to assemble and test what we know about proteins and networks. Models can help address key questions about the measurement, definition and function of proteomic networks. Here, we place these biological questions at the forefront in reviewing the computational strategies that are available to analyze proteomic networks. Recent examples illustrate how models can extract more information from proteomic data, test possible interactions between network proteins and link networks to cellular behavior. No single model can achieve all these goals, however, which is why it is critical to prioritize biological questions before specifying a particular modeling approach.     

Ecological decision-making: From circuit elements to emerging principles

The interactions an animal has with its prey, predators, neighbors, and competitors are known as ecological interactions. Making effective decisions during ecological interactions poses fundamental challenges for the nervous system. Among these are the need to filter relevant information out of complex and ever-changing sensory scenes, to balance competing objectives, and to generate robust behavior amid the strong mutual feedbacks that occur during interactions with other animals. Here, I review recent advancements in the study of ecological decision-making. Using research with fishes, I illustrate how knowledge of ethology and brain circuitry are converging to yield a more holistic understanding of how the brain solves these problems to produce robust sequences of natural behavior.     

Nature-Nurture and the Debates Surrounding Ethology and Sociobiology

The central problem in the history of animal behavior has beenthe inability to perceive the phenotype as the result of aninteraction between genome and environment, despite the considerablelip service paid to the interaction. In North America the comparativestudy of animal behavior was overshadowed by the growth of anexperimental psychology that produced the general-process viewof learning, holding that the mechanisms underlying learningare much the same in all species. That made evolution irrelevant.During the same period ethology emerged in Europe as the studyof naturally occurring behavior in an evolutionary context.Because evolution is fundamental to ethology, the genetic basisof behavior was a central precept. Ethology and psychology collidedafter World War II. After a vigorous exchange on the issues,a synthesis by Robert Hinde materialized, one that advancedthe study of behavior and produced a sophisticated understandingof nature and nurture. A few decades later sociobiology appearedand was immediately assailed for making what were seen as unwarrantedextensions from animal to human behavior, and for emphasizinggenetic control of behavior. Much of the debate that ensuedwas distractingly political and threw little light on the scientificmerits of the issues although it moderated the stance of sociobiologists;on the other hand, the politically inspired debates may haveharmed the field of animal behavior.     

斑马鱼行为学实验在神经科学中的应用

斑马鱼作为新型模式动物的优势正在逐渐被人们所认识,其应用的领域也越来越宽广．斑马鱼在神经生物学中的应用,除了在发育方面比其他模式动物更具优势外,在行为学方面的应用也更加丰富．由于斑马鱼幼体在受精后前两天通体透明,眼睛大小占到大脑体积的二分之一以上,成鱼昼夜节律明显,对光反应强烈,因此斑马鱼在视觉领域应用的优势十分明显．斑马鱼的嗅觉、听觉器官都在体表可见,可以很容易地用行为学实验手段对嗅觉和听觉功能进行检测．斑马鱼习性好动,利用斑马鱼进行运动方面的行为学观察也非常便利．斑马鱼具有群聚习性,在社会生物学研究方面正得到越来越多的关注．斑马鱼行为学是一种比较简单而又有效地分析神经整合功能的方法,并形成了许多相关的实验模型．     

I. P. Pavlov and K. Lorenz

In the thirtieth, the founder of ethology Austrian zoologist Konrad Lorenz put forward the new theory of behavior, which was met with considerable resistance of the dominant views on the mechanisms of behavior, including Pavlov's concept. From his first theoretical works and later on Lorenz debated with Pavlov. However, these debates were not reduced to a disagreement. He appreciated greatly the scientific contribution of Pavlov, and the ideas of the Russian physiologist were often the starting point of his own speculations. His polemics with Pavlov differed very much from his uncompromising controversies with behaviorists. When Lorenz compared Pavlov's views with behaviorism, he often preferred Pavlov's ideas. Lorenz also draw some parallels between the Pavlov's understanding of behavior and the ethological approach. Lorenz's discussion with Pavlov about the nature of conditioned reflex is of particular interest, since it stimulated Lorenz to develop the theory of this phenomenon.     

三种珍稀有蹄类动物的警戒行为数据

警戒行为是野生动物重要的反捕食策略之一, 警戒行为的研究已经成为行为生态学中继动物的采食行为、繁殖行为之外的另一热点研究领域。然而, 尽管研究人员至今已经在数百种鸟类、兽类中开展了各种类型的警戒行为学研究, 但相关研究的原始数据却鲜有共享。本文公开了利用焦点取样法采集的我国3种珍稀有蹄类动物警戒行为数据样本716个, 其中普氏原羚(Procapra przewalskii) 175个、藏原羚(P. picticaudata) 180个、麋鹿(Elaphurus davidiamus) 361个, 并同时公布了采集该行为学数据时的相关变量, 包括性别、群体类型、群体大小、捕食风险、人类干扰等。结果显示在上述3种有蹄类动物中, 均存在明显的集群效应, 且此效应与性别及捕食风险存在交互作用。本文尝试建立标准的行为学数据规范, 以期为未来的行为学研究数据的共享及深度挖掘提供可能。     

On the Problem of Man in Psychology

Very few works in our literature have been devoted to human ethology and social ethology, particularly of children. Psychological-pedagogical approaches predominate; these are based on an assessment of verbal information and on the results of experimental or educational inputs. But such studies should rest on knowledge of the distinctive features of a person's immediate behavior, and these can be ascertained solely through objective study, in which every directed input is precluded.