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A Short History of Studies on Intelligence and Brain in Honeybees Randolf Menzel A short history of studies on intelligence and brain in honeybees Randolf Menzel To cite this version: Randolf Menzel. A short history of studies on intelligence and brain in honeybees. Apidologie, 2021, 52 (1), pp.23-34. 10.1007/s13592-020-00794-x. hal-03320446 HAL Id: hal-03320446 https://hal.archives-ouvertes.fr/hal-03320446 Submitted on 16 Aug 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2021) 52:23–34 Review article * The Author(s), 2020 DOI: 10.1007/s13592-020-00794-x A short history of studies on intelligence and brain in honeybees Randolf MENZEL Berlin, Germany Received 20 February 2020 – Revised 24 June 2020 – Accepted 21 July 2020 Abstract – Reflections about the historical roots of our current scientific endeavors are useful from time to time as they help us to acknowledge the ideas, concepts, methodological approaches, and idiosyncrasies of the researchers that paved the ground we stand on right now. The 50-year anniversary of Apidologie offers the opportunity to refresh our knowledge about the history of bee research. I take the liberty of putting the founding year of Apidologie in the middle of the period I cover here. The nascent period of behavioral biology around the late 19th to the early twentieth century was intimately connected with a loss of concepts related to the mental functions of the brain, concepts that were rooted in Darwin’s theory of gradualism in the living world including cognition in animals. This loss was celebrated both in ethology and behaviorism as the gateway to scientific impartiality. Using this apparently strict scientific approach, impressive discoveries were made by observing and strictly quantifying the behavior of bees. The first forays into the brain, however, uncovered a richness of structure and function that reached far beyond stereotypical input/output connections and opened the way to compensating the conceptual restrictions imposed on us by traditional ethology. Honeybee research provides us with a particularly exciting story in this context. The cognitive turn in behavioral biology is intimately connected to the increasing knowledge of how the brain works, also in honeybee research. What has been achieved so far is just the beginning, but it gives us a glimpse of a promising future. Teamwork between neuroscientists and behavioral biologists is needed to elucidate brain functions such as the expectation of future outcomes and intentionality as an entry to animal intelligence reflecting the flexibility and adaptability in behavior also seen in honeybees. honeybees / intelligence / brain 1. INTRODUCTION look into natural behavior in the species-specific environment and selected those behaviors that AtthetimethejournalApidologie was could be released or induced reliably multiple founded, behavioral biology was comfortably em- times (Tinbergen 1951; Thorpe 1979). Behavior- bedded in two parallel, rather independent streams ists worked preferably in the lab creating condi- of thinking—ethology and experimental psychol- tions that led to repeatable test conditions using ogy (behaviorism, Pavlovian psychology). Al- classified training schemes (Skinner 1988). Al- though there were considerable battles between though the research strategies and terminology the two disciplines, each found itself on a concep- were very different between the two disciplines, tually firm foundation. Ethologists preferred to they had a shared understanding that interpretive or intervening terms, particularly those that included hidden reference to brain functions, Corresponding author: R. Menzel, [email protected] were to be avoided or even banned. Rollin This article is part of the Topical Collection on the (1990) characterized this attitude convincingly as Apidologie 50 Years “how animals lost their minds”.Furthermore,an Handling Editor: Monique Gauthier additional common ground of both schools was 24 R. Menzel their harsh opposition to any form of “anecdotal lancelet, and one of the higher apes, than between cognitivism” and anthropomorphism (Jamieson an ape and a man; yet this interval is filled up by and Bekoff 1996) as entertained by nineteenth numberless gradations.” (p. 445). century zoologists including Darwin (see exem- Ethologists like von Frisch might have argued plary cases below). This victory over the “unsci- that insects and arthropods in general followed an entific attitudes of the past century” was celebrat- evolutionary branch too remote from that of mam- ed whenever the debate about the differences be- mals and primates, and thus, their behavioral strat- tween the two schools became too complicated egies of coping with the demands of the environ- and when doubts appeared about their respective ment involved basically different adaptations, as conceptual delimitations emerged. for example specialized sense organs and highly Insects were thought to naturally belong to tuned adaptations of adjusting instinctive re- the realms of ethology, because their behavior sponses (see below). We might also be surprised was obviously dominated by innate and rather about von Frisch’s statement because he devel- stereotypical routines. Furthermore, insects oped the training method for bees to perfection, have small brains, and thus, cognitive aspects documenting with each experiment how flexible could be more easily dismissed. Von Frisch the bees’ behavior is. While applying these (1962, p. 78) somewhat apodictically stated: methods, he discovered the honeybee’smostim- “The brain of a bee is the size of a grass seed pressive behavior (the waggle dance), which clear- and is not made for thinking. The actions of ly cannot be thought of as an instinctive behavior at bees are mainly governed by instinct”.There all since it is a communication process which is are several reasons why we should be surprised based on learned flight routes embedded in the by von Frisch’s statement. Von Frisch was a memory about the explored environment (see be- highly informed naturalist and evolutionary bi- low). There is also a third reason why we should be ologist. He certainly knew Darwin’s(1859) surprised about von Frisch’s statement. The brain position, as expressed, for example, in the fol- of the honeybee although tiny was wonderfully lowing statements taken from The origin of described as early as the mid-nineteenth century species by means of natural selection or the (Dujardin 1850; Kenyon 1896), and the volume of preservation of favored races in the struggle the whole brain or parts of it (the mushroom body) for life : “… there may be extraordinary mental was related to the social life and the complexity of activity within an extremely small absolute behavior in solitary and social Apoidea (von Alten mass of nervous matter: thus the wonderfully 1910) indicating an intrinsic structure that is diversified instincts, mental powers, and affec- adapted to its functions. tions of ants are notorious, yet their cerebral I have referred to Karl von Frisch at the outset ganglia are not so large as the quarter of a small of this review because he is the most eminent pin’s head.” And “There is no fundamental honeybee researcher of the last century, and also difference between man and the higher animals because I had the privilege of talking to him in their mental faculties” (p. 448). He claimed (though only briefly) in 1965. Obviously, we have that “the lower animals, like man, manifestly to reach beyond the last 50 years of honeybee feel pleasure and pain, happiness, and misery.” research in order to better understand the concep- (p. 448). And: “If no organic being excepting tual framework in which behavioral and neurobi- man had possessed any mental power, or if his ology developed in the first and the second half of powers had been of a wholly different nature the twentieth century. from those of the lower animals, then we should never have been able to convince ourselves that 2. ARE BEES INTELLIGENT, AND our high faculties had been gradually developed. WHAT IS INSECT INTELLIGENCE? But it can be shown that there is no fundamental difference of this kind. We must also admit that Although nineteenth century naturalists and there is a much wider interval in mental power honeybee lovers were excellent observers, they between one of the lowest fishes, as a lamprey or were criticized for two inexcusable failures: A short history of studies on intelligence and brain in honeybees 25 reporting only single case events and using unjus- specific adaptations but also the quantification tified anthropomorphic terminology. Indeed, rep- process itself. Similar doubts were raised much etitions under strict experimental control were later with respect to learning functions and mem- rarely performed, and, if so, the conditions were ory span and brain size (Rensch 1954). not reported. Anthropomorphic terminology was Learning during departure. “As the bee takes not considered misleading or dangerous because off she turns her head towards the hive and, while Darwin’s gradualism guided the comparative ap- continuously hovering up and down, she inspects proach in behavioral studies as in comparative in detail the hive itself, the neighboring hives and morphology. Reading this literature gives the the hive stand, all the while directing her eyes strong impression that the authors, such as towards the hive. Only after this prelude are first Romanes (1883), Forel (1910), Buttel-Reepen small and then ever-increasing orientation circles (1900), and even Maeterlinck (1901) with his traced and thereby the immediate and more distant romantic style in praise of the honeybee, did not surroundings memorized” (Buttel-Reepen 1900, mean mental operations of a human kind when p.
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