Playing, an everyday life activity: easy to spot, hard to define

After focusing for a long time on animal grief, trauma, violence, pain and suffering, comparative psychologists have been lately putting their efforts into dealing with happiness, laughter, joy and affection both in humans and other animals (the so-called ‘positive psychology’). Most of the ‘positive emotions’ which are under the psychologists’ magnifying glass are also indissolubly linked to play. Every day of our lives is punctuated by play and humour. We play during conversation with friends on the phone or on Skype, or when we post messages on Facebook – frequently inserting a smiling face like this :-) – etc. We play with our conspecifics and also with members of other species. Dogs, cats and even rats can be wonderful playmates. We play because it is pleasurable and rewarding. By social play and humour we experience emotions that can pass individuals’ boundaries and create a network of social and affective bonds (Power, 2000). Despite its pervasive nature, play is one of the most mysterious behaviours an ethologist can come across.

The difficulty with studying play behaviour starts with its theoretical definition. In his Confessions (Book 11, Chapter 14), St Augustine pondered the meaning of time, ‘Quid ergo est tempus? Si nemo ex me quaerit, scio: si quaerenti explicare velim, nescio’ [What is time? If no one asks me, I know. If I want to explain it, I no longer know]. Maybe the frustration experienced by St Augustine is the same as that experienced by most ethologists when dealing with the definition of play (Palagi and Paoli, 2007, 2008). We have no problems in recognising a playful interaction of our dogs, cats and children; however, as we go through the extensive literature dedicated to play we soon realise that there are as many definitions of play as there are the authors who studied it (for an extensive review see Burghardt, 2005). Play has been often defined via litotes, by not specifying what it is but by specifying what it is not. As play lacks certain characteristics that are typical of the serious and functional behaviours, play has been defined as a non-functional behaviour with no obvious immediate benefits (Martin and Caro, 1985; Bekoff and Allen, 1998).

What is multimodal communication?

The American journalist Sydney Harris briefly and effectively tagged the difference between information and communication. According to common definitions, information refers to facts about a situation, an individual or an event. Communication is ‘the process of sharing information, especially when this increases understanding between people or groups’ (Cambridge Dictionary) or ‘the imparting or exchanging of information by speaking, writing, or using some other medium’ (Oxford Dictionary). These definitions are centred on human communication when, in fact, communication is a widespread – and necessary – phenomenon spanning the whole animal kingdom. The light pulses of fireflies (Bradbury and Vehrencamp, 1998), the dance of honeybees (von Frisch, 1967; Seeley, 1997), the claw-waving displays of crustaceans (Dingle, 1969), the songs of birds (Vehrencamp, 2000), the alarm calls of different primates (Cheney and Seyfarth, 1990), and the articulate language of humans (Savage-Rumbaugh et al., 1998) are just some examples of information transmission between or among conspecifics.

Communication is an essential prerequisite for sociality and has evolved along with the development of social systems, from the simplest to the most complex (Freeberg et al., 2012). Communication involves the transmission of a signal, which is any action or trait produced by one animal, the sender, that provides information used by another animal, the receiver (Wilson, 1975; Endler, 1993; Hebets and Papaj, 2005). A signal is complex if it can be disassembled into different, single components, each of them able to elicit a response in the receiver. Such a response, of course, can be different from the response elicited by the complex signal. For example, when the telephone rings we stop doing what we are doing to answer. So, the ring has elicited a response in the receiver (us). Once we have picked up the phone, we can just hear a beep sequence if the signal is lost or we can hear the voice of a friend and start a conversation.

Biological (or pseudo-cultural?) market

It is well known that both Darwin and Wallace were influenced by the work of the economist and demographist Thomas Malthus (An Essay on the Principle of Population, published in 1797) while elaborating their theories on evolution. Probably, the mechanisms underlying the economic system are the outcome of an evolutionary process, which has acted on the biological system and reflects on our behaviour. The analogy between economical and biological systems is not limited to this example. In biology, as well as in economics and politics, power is a key concept for understanding asymmetric relationships between subjects (Dahl, 1957). Distributive power, derived from Russell's definition of social power (1938), focuses upon who has got the power over whom. It can originate from coercion, when an individual can force another to do something, or from leverage, when the use of force is not possible. Specifically, coercive power depends on fear, suppression of free choice and/or use of threat, for its existence. It is normally based on an imbalance of social, psychological and physical power between individuals. Examples of this kind of power are theft with violence to obtain valuable goods (Matsueda et al., 2006), bullying to aggressively impose domination over others (Rayner and Hoel, 1997) and rape (Thornhill and Thornhill, 1983; Emery-Thompson, 2009; Muller and Wrangham, 2009). Human, gorilla, chimpanzee and orangutan males perform sexual coercion over females to obtain forced copulations (Goetz and Shackelford, 2006; Muller and Wrangham, 2009). Wild orangutans provide one of the most dramatic examples of this phenomenon. It has been reported that in this species ‘most copulations by subadult males and nearly half of all copulations by adult males occur after the female's fierce resistance has been overcome through violent restraint’ (Smuts and Smuts, 1993, p. 6). Sexual coercion is also present in many other animals spanning invertebrates and mammals. It is worth mentioning, among others, that scorpion flies (Thornhill, 1980), guppies (Head and Brooks, 2006), salamanders (Ethan et al., 2006), snakes (Shine and Mason, 2005), mallards (Barash, 1977), bottlenose dolphins (Scott et al., 2005), and a huge variety of non-human primates (Smuts and Smuts, 1993) force their mates into sex.

In 1960 Dr Louis Leakey, palaeontologist and anthropologist, suggested that I should travel to the Gombe National Park, in what is now Tanzania, to study the behaviour of the chimpanzees there. He believed that apes and humans shared a common ancestor some 6 or 7 million years ago and that an understanding of chimpanzee behaviour in the wild might help him better understand how our prehistoric ancestors may have behaved. Subsequently, when I had been in the field for some 18 months, he arranged for me to go to Cambridge University to work for a PhD (although I had never been to college). In the early sixties ethologists tended to be reductionists, searching for simple explanations for very complex behaviours. When I talked about the Gombe chimpanzees having different personalities, complex cognitive abilities, minds, and emotions such as pleasure and sadness, anger, frustration and so on, I was accused of anthropomorphism as those attributes, I was told, were unique to the human animal. Some scientists were even shocked that I referred to the chimpanzees by names rather than numbers. Fortunately, I had learned from my dog, as a child, that none of that was true.

Since those days the science of animal behaviour has come a long way and there have been many studies of animal cognition, animal emotions and even personality. In other words the sharp line once believed to separate humans from the rest of the animal kingdom was blurred. There was a difference of degree between the behaviour of humans and chimpanzees, but not of kind. Since then other studies have shown that many of the complex behaviours shared by the great apes and humans are present also in monkeys. And during the last decade the barrier between monkeys and lemurs has also been found to be increasingly fragile. Lemurs – the spirits of our ancestors according to some Malagasy traditions – exchange services, suffer and manage anxiety, reconcile, and use play to increase tolerance towards unfamiliar individuals.

Many species of lemurs are extremely endangered, and an understanding of their behaviour, in addition to helping us to understand the origins of some of our own behaviour, is also crucial for determining the best conservation strategies. We need to understand how the lemurs interact with each other and with their forest environment.

Individual recognition: why and how

Human society is founded on individual recognition. The distinction of ‘others from others’ rules every aspect of a community, from the personal to the social level. In his ‘The Man Who Mistook His Wife for a Hat’, Oliver Sacks (1970) stresses how the ability to discern individuals is crucial to make a judgement over them and their true identity. Understanding individuals’ uniqueness is pivotal to choose partners and friends, care for family members, vote for a candidate, form political alliances, seal trade agreements, and follow rock icons or religious leaders. Individual recognition is not unique to humans. It is, instead, an ancient cognitive skill shared with other primates and rooted in humans’ mammalian history. From lemurs to apes, such ability is critical, for example, to select mates and supporters, form parent–offspring bonds, establish dominance relationships, set up coalitions, exchange or interchange commodities and follow group leaders (Thom and Hurst, 2004). Individual recognition is an excellent example of the cognitive continuity that bridges humans and other primates.

Individuals can be discriminated according to their unique features, or cues. Different from signals, specifically designed to convey information beneficial to the sender (Bradbury and Veherencamp, 1998), cues carry potential information whose relevance depends on the receiver. Paradoxically, the same cue can mean something for one animal and nothing for another which does not read the cue as a cue at all! Consequently, defining a cue is not easy.

We human beings are distinctly unusual in the way we behave, and most particularly in the way in which we process information about the world around us. The final finishing touches to the distinctive manner in which we think and interact seem to have been acquired rather recently. But they were based upon, and made possible by, a complex biological edifice that had been under construction for a very long time indeed. If anything that happened along the winding road of primate and human evolution had failed to happen, for whatever reason, we would not be the creatures we are today. As a result, we are not only who we are, but we are also who we were. Arguably, that long history stretches back to the very beginnings of life on planet Earth; but probably the most useful place to start any rational account of it is with the origin and early evolution of our own unique mammalian order, Primates.

The primate – and ultimately human – edifice has been built, incrementally, over the past sixty million years or so. The foundations and lower floors of that edifice were furnished by the early primates, whose fossils we know from North American, Eurasian and African rocks dating between about sixty and forty million years ago. But these forms are long vanished; and the closest thing we have to living, observable, analogies for those ancient relatives are the strepsirrhine primates of the tropical Old World. Also including a handful of nocturnal species from tropical Africa and Asia, the strepsirrhines are incomparably well represented by the lemurs of the mini-continent of Madagascar. Isolated in their island domain for upward of fifty million years, the lemurs have radiated into an astonishing array of adaptive types: large and small, nocturnal and diurnal, suspensory and cursorial, leaf-eating and fruit-eating, highly arboreal and at least partly terrestrial, eurytopes and stenotopes, gregarious and solitary. Sadly, the larger-bodied representatives of this amazingly diverse and apparently monophyletic primate group are recently extinct, at least partly due to the depredations of humankind. But the surviving species, reckoned to number between fifty and a hundred, depending on the criteria you use to recognise them, still present us with a mind-boggling adaptive diversity.

When we started considering the idea to write this book on lemurs’ behaviour in 2010 we thought of making reference to the relatively few experimental studies on lemur cognition in the introduction, mentioning them as a promising novel branch of investigation for strepsirrhines. But over the past few years the research on the subject has blossomed and many articles have been published on scientific journals, converting the lemur cognition domain in one of the most flourishing fields of investigation of primatology, anthropology and comparative psychology. We realised, then, that we could not dismiss cognitive studies with a couple of paragraphs in the introductory section and we decided to reserve the final chapter to the topic, which probably better than others points towards unexplored lemur potentials and future directions for a more comprehensive understanding of the primate world. In the following pages we try to provide the reader with the basic elements that we think are necessary to understand what is going on when lemurs are tested on cognitive tasks. We suggest that the reader uses this chapter for orientation, as a sort of compass to navigate through the different aspects of lemur cognition. If it is of interest, we invite the reader to consult the original papers to gather further details on the experimental apparatuses and procedures.

Manipulative lemurs? Maybe

In her 1966 Science article, Alison Jolly observed that ‘some prosimians, the social lemurs, have evolved the usual primate type of society and social learning without the capacity to manipulate objects as monkeys do. It thus seems likely that the rudiments of primate society preceded the growth of primate intelligence, made it possible, and determined its nature’.

As primatological studies have advanced, some evidence of tool manipulation ability, a possible precursor of tool use, has been found in lemurs (for a review see Fichtel and Kappeler, 2010; Schilling, 2013). Only few incidents of spontaneous object manipulation have been observed in the wild. The aye-aye (Daubentonia madagascariensis; Figure 9.1) is known for using the probing middle finger for tapping, and extracting nectar, kernels and insects embedded in trees or branches; it can also use the fourth finger for tasks requiring strength, scooping action and deep access (Lhota et al., 2008).

Theoretical discussion and debate are open on which part of social behaviour is really exclusive of Homo sapiens and other apes, and what, instead, is rooted in the common ground of primate origins. Since the time of our common ancestors, lemurs have been following their own evolutionary pathway to become ‘modern primates’. This process, enhanced by Madagascar's isolation from the rest of the world, which started about eighty million years ago, has led lemurs to possess a puzzling combination of features, such as a small brain and communication highly based on smell combined with biological peculiarities, such as female dominance, lack of sexual dimorphism and strict seasonal breeding. On the other hand, group-living lemurs share basic features with social monkeys and apes such as cohesive multimale-multifemale societies, female philopatry and individual recognition. Lemurs are the ideal model to shed light on the ‘primate behavioural potential’ in terms of conflict management, communication strategies and society building, and on how much these crucial aspects of social living are similar to or different from those found in monkeys, apes and humans. Part of the perceived gap between strepsirrhines and haplorrhines – also mentioned by Alison Jolly and Ian Tattersall in their foreword – probably lies in the divergent research methodologies applied to these two groups. The aim of this book is to review and expand upon the newest fields of research in lemur behavioural biology, including recent analytical approaches that, so far, have been restricted to haplorrhines.

Breaking the wall

Are lemurs primates? This question may sound rhetorical, but unfortunately the answer (yes, they are) cannot be taken for granted.

The idea for this book came to our minds after a few influential Italian anthropologists had questioned the relevance of lemur behavioural studies to the anthropological domain and, therefore, to the understanding of the evolution of human behaviour. Monkeys were discriminated against as well, because – according to these scholars – they did not fit in the discipline, unless direct comparisons with humans were drawn. While the significance of lemurs and monkeys to human evolution was debated (and no consensus reached), apes were automatically included in the anthropological domain, thankfully. Of course the discrimination of strepsirrhines and monkeys was instrumental in favouring other research strains.

Upright habits and their impact on sexual signalling

In a number of animal species, it is possible to observe that males and females strongly differ in specific morphological and/or behavioural traits. This phenomenon, called dimorphism, can be largely observed in primates showing male–female differences in parental investment, growth and developmental pattern, body and canine size, scent glands and scent marking behaviour, vocalisation and visual ornaments (e.g., skin colours, flanges and fur). Such sexually dimorphic features are defined as ‘secondary’ because they are under the hormonal control of primary sexual characters (reproductive organs). Therefore, secondary traits are not primarily involved in the production of offspring. Not only do they not appear to promote the survival of individuals but sometimes they appear to be detrimental to the animal which possesses them; for example, colourful ornaments (such as the notorious peacock tail) can increase animal visibility and predation probability and, consequently, reduce the chances of survival.

Since secondary sexual traits do not confer advantages or produce disadvantages, their evolutionary permanence is in apparent contrast with the classic natural selection theory proposed by Darwin in the Origin of Species (1859). Why have secondary sexual traits been selected, then? To explain this paradox, Darwin (1871) developed the theory of selection in relation to sex (sexual selection) which pivots around the fact that secondary sexual traits confer an advantage with respect of acquiring a mate by intimidating rivals and/or by attracting mates. In this respect, the race to maximise offspring production – promoted by sexual selection – is as important as the race to maximise survival chances – promoted by natural selection. According to a convincing recent theoretical synthesis, sexual selection is part of natural selection (Clutton-Brock, 2004) intended as a process aimed at increasing an animal's chance of surviving and producing the highest number of offspring.

Stress, anxiety and…evolution

Back in 1872, Darwin, in The Expression of the Emotions in Man and Animals, wrote about emotion expression as the possible result of ‘the direct action of the excited nervous system on the body independently of the will’. In the whole animal world, bodily movements are able to reveal and unveil emotions not apparent otherwise. In humans, gestures, facial expressions and, more in general, non-verbal behaviours are an integral part of how we express our emotions. Emotions include anxiety, which can be linked to fear, motivational conflict, or uncertainty in decision-making (Morgan, 2006).

Defining anxiety is not easy, as also recognised by Sigmund Freud back in 1920 (see the 1969 edition). Linguistically speaking, anxiety is defined as a ‘…feeling of nervousness or worry about something that is happening or might happen in the future’ or, similarly, ‘a feeling of worry, nervousness, or unease about something with an uncertain outcome’. Stress is defined, instead, as ‘great worry caused by a difficult situation, or something that causes this condition’ or ‘a state of mental or emotional strain or tension resulting from adverse or demanding circumstances’ (definitions by Cambridge and Oxford online dictionaries, respectively). From these non-technical definitions, it is possible to infer intuitively that anxiety can be related to stress but also that the difference between stress and anxiety is not clear-cut. Indeed, a plethora of models, theories and hypotheses have been put forth to integrate stress and anxiety into a single framework. However, the behavioural, physiological, psychological and clinical implications of anxiety and stress responses have proven difficult to untangle.

In Homo sapiens, non-human primates and other mammals, anxiety is an emotional state involving tension and/or agitation, with both physiological and behavioural implications (van Riezen and Segal, 1988; Craig et al., 1995; Barros and Tomas, 2002; Bourin et al., 2007). Indeed, anxiety is associated with a characteristic set of behavioural responses, including avoidance, vigilance and arousal, which evolved to protect the individual from danger (Gross and Hen, 2004).