綜合論述 台灣昆蟲 31: 85-99 (2011) Formosan Entomol. 31: 85-99 (2011) How Human Are Insects, and Does it Matter? Thomas F. Döring1, and Lars Chittka2* 1 The Organic Research Centre, Elm Farm, Hamstead Marshall, RG 200HR, UK 2 Queen Mary University London, School of Biological and Chemical Sciences, Biological and Experimental Psychology Group, Mile End Road, London E1 4NS, UK. ABSTRACT Over the past two decades, a wealth of information on cognitive function in insects has been generated and this work has been tremendously useful in pinpointing just how much can be done with how little neural circuitry in miniature brains. However, other recent claims on the occurance of ‘teaching’, ‘culture’, ‘consciousness’, or ‘personality’ in the insects seem to apply a relatively restrictive top-down approach, where researchers set out to discover human-like behaviours in animals. This approach is prone to terminological ambiguities, because terms taken from the domain of human experience often invoke more complex connotations than the restricted criteria used to test the phenomena in the animal world would permit. It also bears the risk of circularities as a consequence of selecting and shaping definitions and test criteria. Finally, the hypothesis-driven approach may be vulnerable to research biases, such as to predominantly report positive results or to mainly investigate “clever” animals. We suggest that the current approach needs to be supplemented by a complementary modus operandi. In a more exploratory, bottom-up ‘ethomics’ approach, psychological constructs would only emerge after multivariate data analysis of a broader range of animal behaviours. It is also necessary to consider the process of how we arrive at definitions as part of the research methods. Key words: ambiguity, arbitrariness, behaviour, cognition, methods, terminology Introduction might be considered uniquely human domains: agriculture, slavery, territorial wars, castes, Some of the attraction for scientists to division of labour, consensus building, a the insects, especially the social ones, is symbolic language, and teeming cities undoubtedly that they have evolved a with fantastic architecture (Lindauer, number of feats that, to a non-biologist, 1955; Frisch, 1967; Hölldobler and Wilson, *Corresponding email: [email protected] How Human Are Insects, and Does it Matter? 85 1990). However, there is perhaps little fundamental conceptual problems in animal scholarly information to be gleaned from cognition science could be seen in the such similarities: insects and humans are predominant approach of reducing complex too distantly related for such comparisons behavioural or psychological constructs to reveal anything but evolutionary into small sets of experimental test criteria. convergence. The terms that label these We will explore the consequences of this features are merely metaphors, and they top-down approach and compare it to an should not mislead us to construe that alternative, bottom-up approach, thereby insects ‘think‘ like humans. However, in touching on questions of terminological recent work on insect cognition, the ambiguities, the arbitrariness of definitions, boundaries between human and insect and problems of undetected circular reasoning. performances have often been blurred, sometimes in ways that are not just The top-down approach in innocent metaphors. There is no question animal cognition that some insects perform impressive cognitive feats; recent discoveries include Current work on animal cognition, attention-like processes (Spaethe et al., where it is dealing with psychological 2006; Van Swinderen and Andretic, 2011), constructs, typically follows a type of categorization of visual stimuli (Zhang et hypothesis-driven approach that is ‘top- al., 2004), rule learning in delayed matching down’ in more than one way. First, concepts to sample tasks (Avarguès-Weber et al., and terms are mainly anchored in human 2011), context learning (Collett et al., psychology, and then superimposed on 1997), sequence learning (Chittka et al., animals. Second, the hypotheses are often 1995), various types of social learning not strictly deductive, as good hypothesis- (Leadbeater and Chittka, 2007), interval testing might be; instead the hypothesis is timing (Boisvert and Sherry, 2006), often that animals exhibit behaviour that associative recall (Reinhard et al., 2004) is human-like, and researchers are content and sensitivity to number (Chittka and with confirming this hypothesis, and indeed Geiger, 1995). However, other recent claims with adjusting both procedures and definitions on the occurance of ‘teaching’, ‘culture’, to see it confirmed. ‘consciousness’, or ‘personality’ in the insects The top-down approach in animal seem to apply a relatively restrictive top- cognition relies on taking interesting down approach, where researchers set out psychological constructs that are rooted in to discover human-like behaviours in animals. the human domain, and translating these This approach is prone to terminological into experimental paradigms for animals. ambiguities, because terms taken from the The constructs have acquired their names domain of human experience often invoke in the human world, not in the zoological more complex connotations than the restricted sciences, and an almost inevitable consequence criteria used to test the phenomena in the of this is terminological confusion, i.e. the animal world would permit. chosen terms are ambiguous. Certainly, Bordering on psychology, philosophy, this hypothesis-driven way of conducting physiology and ecology, the science of animal research on animal cognition is very cognition attracts interest from many sides. powerful and has fuelled massive progress Since all bring in their terminological in the understanding of animal behaviour traditions, cross-discipline communication and animal cognition over the last few can be difficult. However, this is not the decades (Bekoff et al., 2002). Nothing can only, and possibly not the most serious beat the excitement accompanying the source of conceptual confusion. In this successful completion of a rigorously paper we argue that one of the most designed experiment that proves the 86 台灣昆蟲第三十一卷第二期 existence of a cognitive ability in an predisposition to think, feel, and act in a animal species for the first time. Pointing particular way. To still others, personality out problems in this approach, therefore, consists of a person’s unique mixture of may carry the risk being regarded as a emotional, intellectual, and character traits spoilsport activity (Shettleworth, 2010). (honesty, courage, etc.). To more behaviorally However, we believe that it is worth oriented psychologists, personality is not taking this risk for the potential reward of something internal, but rather an externally new insights into the world of animal (and observable pattern of organized behavior specifically insect) cognition. typical of a person. Perhaps an acceptable compromise is to define human personality Terminology: the problem of ambiguity as a composite of cognitive abilities, interests, and content erosion attitudes, temperaments, and other individual Some terminological inaccuracies are differences in thoughts, feelings, and behavior. innocent. When the words ‘queen’, or This definition emphasizes the fact that ‘honeybee dance’, or indeed ‘dance language’ personality is a unique combination of are used in studies of social insects it is cognitive and affective characteristics clear that the double meaning of the words describable in terms of a typical, fairly will not endanger the conceptual clarity of consistent pattern of individual behavior. entomological studies. The semantic distance From the last definition, it follows that of the word ‘queen’ between the worlds of methods of assessing personality should insect and human societies is too large to include a broad spectrum of cognitive and lead to any misunderstandings. Thus, the affective variables.” (Aiken, 2000) metaphorical use of these anthropo- In humans, personality is now often morphisms is safe. Just using the word quantified in terms of the ‘big five’ ‘queen’ in the title of a bee study does not dimensions openness, conscientiousness, offer any increased attention from readers. extraversion, agreeableness, and neuroticism In contrast, consider the question (Goldberg, 1993), where each of these is whether the individuals of certain animal explored using a multitude of questionnaires species can be said to have ‘personality’. or tests. Contrast this complex picture of This term, without inverted commas, is personality, emphasizing the plurality of now commonly used among vertebrate approaches, with the approach to measure behavioural ecologists (Bell and Sih, 2007; the correlation between just two behavioural Frost et al., 2007), and this has recently variables in ‘personality’ studies in animals expanded into the insect literature (Wray (Bell and Sih, 2007), or indeed just a basic et al., 2011), with the curious implication level of consistency in a single behavioural that insects have person-like qualities. trait (see e.g., references in Muller et al., Although the term may be defined concisely 2010). To add to the confusion, some in an animal study, its grandeur, which authors use the terms “personality” and has been acquired in psychology, may spill “behavioural syndrome” interchangeably, over into the world of insects – at the whereas others make a distinction (Dall et considerable risk that meanings are al., 2004; Sih et