Marc Bekoff (Marc Bekoff is a professor in the Department of Environmental, Population and Organismic Biology at the University of Colorado, Boulder. His book "The Smile of A Dolphin: Remarkable Accounts of Animal Emotions" will be published later this year by Random House/Discovery Books)

     HIGHLIGHT: Are humans the only animals that feel emotions ? Besotted whales, ecstatic iguanas and embarrassed chimps have persuaded Marc Bekoff and other biologists that we are not alone

     IT STARTED with a touch. Soon Butch and Aphro were slowly caressing. Then they rolled together and embraced, locking flippers, before rolling back again. For perhaps three minutes, the two southern right whales lay side-by-side, ejecting water through their blow holes. The cetaceans then swam off, touching, surfacing and diving in unison. As he watched, Bernd Wuersig of Texas A&M University became convinced that Butch and Aphro were developing a powerful mutual bond. Could this be leviathan love ?

     That's a controversial question. Biologists disagree about the nature of emotions in nonhuman animals, and especially whether they consciously experience their emotions. Many would not dare to say that a whale can fall in love, but those like Wuersig, who do not dismiss this idea out of hand, can trace their thinking back at least as far as Charles Darwin. In "The Expression of the Emotions in Man and Animals", he argued that there is continuity between the emotional lives of humans and other animals. Elsewhere, Darwin wrote: "The lower animals, like man, manifestly feel pleasure and pain, happiness and misery."

     Despite Darwin's interest in the subject, we still don't know much about which animals have emotional lives and which do not. Perhaps this failure to make much headway can be put down to researchers' fear of being labeled "non-scientific" or too anthropomorphic. But the tide is turning. Nowadays it is permissible to ask such questions as: do animals love one another, do they mourn the loss of friends, and do they feel embarrassment ? Current research in animal behavior and neurobiology is providing compelling evidence that at least some vertebrates feel a full range of emotions from fear and disgust to joy, jealousy, anger and compassion.

     Emotions are difficult to pin down. I know they are real because I experience my own every day, but I have no way of knowing exactly how you feel. You might try to describe your emotions using words, but even if you don't, I can deduce something about your emotional state from your body language and behavior. It is the same with animals - strong clues about what they are feeling can be gleaned from changes in muscle tone, posture, gait, facial expression, pupil size, gaze, vocalizations and odors. You don't have to be an expert to read the signs. People with little experience of observing animals usually agree about what they are seeing. And the subsequent behavior of animals often suggests they are correct.

     Behaviour speaks volumes about animal emotions because emotions are psychological phenomena that help an individual to manage and control its actions. Investigating what is going on in the brain, however, is more tricky. From a neurological perspective, it is useful to divide emotions into two types. The most basic, or primary emotions, are innate - they do not require conscious thought or feeling. These emotions are likely to be widespread in the animal kingdom, because they tend to increase an individual's chances of survival. More contentious is the idea that animals also have secondary emotions - the ones that require more sophisticated mental processing.

     The most obvious example of a primary emotion is the fight-or-flight response, which allows animals to react quickly to danger signs, often with no indication that they feel fear. For instance, a young goose that has never been exposed to predators will run and take cover when it sees a hawk-like silhouette overhead, but will not respond to the outline of a goose. Natural selection favours those individuals who react in this way - and the faster the better. A hawk can swoop down rapidly and pluck a gosling while it is still thinking about what to do, so one that avoids the predator by instinct alone has a greater chance of surviving than one that takes time to decide on a response.

Smell of fear
     Sounds and smells can also trigger primary emotions, including innate fear. Domestic dogs are among the many animals that have hard-wired responses to some odours. My companion dog, Jethro, is normally comfortable visiting the vet, but he will show signs of fear if he goes into an examination room where the previous canine client was afraid. It is an instinctive response to a pungent odour released by the anal glands of the frightened dog. Similarly, lab rats that have never encountered cats or other predators show innate freezing responses to the smell of these animals. Even pieces of cat hair seem to cause anxiety - the rats play and eat less, and are more wary than usual.

     Neurobiologists have tracked primary emotions down to an evolutionarily ancient part of the brain called the limbic system, and in particular to a small almond-shaped structure known as the amygdala. This so-called "emotional" brain, which is thought to have evolved to allow sophisticated analysis of smells, is found in fish, amphibians, reptiles, birds and mammals. The amygdala receives raw sensory information from the thalamus - a neural relay station - and is connected by a bundle of nerves to the brainstem, which allows it to prime the body for fast action.

     Speed is essential in a survival situation, but the downside of primary emotions is their inflexibility. That's where secondary emotions have the edge. They involve higher brain centres in the cerebral cortex, allowing an individual to reflect and weigh up the relative benefits of different actions in specific circumstances. We don't know which animals other than humans are capable of conscious reflection about their emotions. But the brain structures and biochemistry that are associated with so-called "felt emotions" in our own species are found in others. This has led some researchers to become convinced that secondary emotions are unlikely to be unique to humans.

     If we accept that we are not alone in experiencing emotions, where can we draw the line ? New findings suggest that reptiles may have been the first animals to experience their emotions. Last year Michel Cabanac from Laval University in Canada showed that iguanas try to maximise sensory pleasure - they prefer to stay warm rather than venture out into the cold to get food. And when basking in a warm environment, they experience physiological changes associated with pleasure in humans and other vertebrates, such as "emotional fever" - a boost in body temperature - and a raised heart rate. Amphibians and fish do not exhibit these behavioural and physiological responses. Cabanac suggests that the first mental event to emerge into consciousness was the ability of an individual to experience the sensations of pleasure or displeasure. His research suggests that reptiles experience basic emotional states, and proposes that such emotions evolved somewhere between amphibians and early reptiles.

     Many vertebrates seem to be motivated by pleasure and nowhere is this more apparent than in their play. There's no doubt that animals at play appear to be having fun. Young dolphins often dart about in the water and also seem to enjoy slowly drifting in the current. Buffaloes have been known to go ice-skating, excitedly bellowing "gwaaa!" as they slide across the frozen ground. I once observed a young elk in Rocky Mountain National Park, Colorado, running across a snow field, jumping and twisting its body while in the air, stopping, catching its breath, and doing it again and again. There was plenty of grassy terrain around but the elk chose the snow field.

     It certainly looks as though these animals are enjoying themselves, and there are some neurobiological findings that support the inferences. Studies of the chemistry of play indicate that it is fun. Jaak Panksepp from Bowling Green State University, Ohio, has found evidence that rats produce opiates during play. They also have increased dopamine activity in their brains when anticipating play, according to findings made by Steven Siviy from Gettysburg College, Pennsylvania. In humans, both opiates and dopamine are associated with pleasure.

     Play is important in development because it teaches a young animal skills that it will require to survive as it becomes independent. If animals play because they enjoy it, then the positive emotions associated with play have an evolutionary advantage just like the fight or flight response. A similar argument has been used to explain what looks like romantic love among animals.

Birds do it.
     Bees may not do it, but birds certainly seem to. Ravens fall in love, according to renowned biologist Bernd Heinrich from the University of Vermont, Burlington, who has studied and lived with these birds for many years. In his book, "Mind of the Raven", Heinrich writes: "Since ravens have long-term mates, I suspect that they fall in love like us, simply because some internal reward is required to maintain a long-term pair bond."

     In many animals, including southern right whales, romantic love seems to develop during courtship and mating. Often this is protracted, with both parties performing rituals that take time and energy and can be risky. It is as if they need to prove their worth to each other before consummating their relationship. Interestingly, our closest living relatives, chimpanzees, don't appear to fall in love. And male chimps don't spend much time courting, mating, or remaining with the females whose young they have fathered.

     Many things have passed for love in humans, yet we do not deny its existence. It is unlikely that romantic love first appeared on the scene in humans with no evolutionary precursors. Many birds and mammals share the brain systems and chemistry that underlie love in humans. Dopamine levels, for example, are elevated in lusting, love-struck humans and in rodents anticipating a sexual encounter. In addition, mammals have the hormone oxytocin, secreted by the pituitary gland, which is associated with courtship and sex. Birds and reptiles have a similar chemical, vasotocin, associated with comparable behaviors. Taken together, these findings suggest that at least some animals are capable of romantic love.

     The flip-side of love is grief at the loss of a loved one. Some animals display the characteristic behaviour we associate with grief. Often there is a period of mourning. Grieving animals may withdraw from their group, sit in one place and stare into space as if they were paralysed. They remain unresponsive to attempts by others to interact with them or console them. They may also stop eating, lose interest in sex, or become obsessed with the dead individual. Some even try to revive the corpse or carry it around until it decomposes.

     Sea lion mothers, watching their babies being eaten by killer whales, squeal eerily and wail pitifully. Dolphins have been seen struggling to revive a dead infant. At the Gombe Stream National Park in Tanzania, primatologist Jane Goodall observed Flint, an eight-year-old male chimp, withdraw from its group, stop feeding and finally die after the death of his mother, Flo. Elephants may stand guard over a stillborn baby for days maintaining a quiet vigil with their head and ears hung down. And young elephants who witness the death of their mothers often wake up screaming. Joyce Poole, who has spent decades studying elephants in the wild, is convinced the orphans experience grief and depression.

     Even birds appear to grieve. "A greylag goose that has lost its partner shows all the symptoms that John Bowlby has described in young human children in his famous book "Infant Grief"," wrote Nobel prizewinning ethologist Konrad Lorenz. "The eyes sink deep into their sockets, and the individual has an overall drooping experience, literally letting the head hang."

     A bereft greylag goose may behave like a bereft human, but does it feel grief in the way that a person does ? This question is difficult to address because we don't yet have a biological explanation of how humans experience their emotions. Antonio Damasio from the University of Iowa offers one possibility in his book, "The Feeling of What Happens", published last year. He suggests that some parts of the brain map both the internal state of our bodies and external objects or situations that are affecting us. Damasio believes that the physiological processes that accompany emotions are not mere by-products, but instead are part of the mechanism that produces feeling. By simultaneously mapping our internal and external environments, we feel our experiences as our own. If Damasio is correct, then his explanation may also apply to some animals, particularly our closest living relatives, the other primates.

     Chimpanzees, for example, may not fall in love but they do appear to experience a wide range of emotions, including embarrassment, which requires an individual to wonder what others are thinking about it. Goodall has witnessed embarrassed chimps. She describes a young male showing off by swinging on a sapling in front of a dominant male. When the branch snapped, the youngster fell head first into long grass. He then turned to check that his fall had not been spotted, climbed another tree and began feeding.

     Another noted primatologist, Marc Hauser from Harvard University, has observed embarrassment in a rhesus monkey. After copulating, the male strutted away and accidentally fell into a ditch. Hauser recounts how the monkey stood up and quickly looked around. After sensing that no one had seen the tumble, he marched off, back high, head and tail up, as if nothing had happened.

     These observations suggest that the differences between human and animal emotions are often differences in degree rather than differences in kind. Even where the similarities with ourselves are not so obvious, if we accept that animals have feelings too, then there are important implications for the way we behave towards them. When animals are seen as automatons with no emotions, it is easy to treat them as mere property with which humans can do as they please. But view them as sentient, feeling individuals and it is more difficult to justify some of our cruel and unthinking practices.

     If we close the door on the possibility that many animals have rich emotional lives - which may be very different from our own - we will lose great opportunities to learn about the lives of creatures with which we share this magnificent planet. There are many mental worlds beyond human experience just waiting to be explored.

Further reading: "Emotion and phylogeny", by Michel Cabanac, "Journal of Consciousness Studies", vol 6, p 176 (1999)

"The Expression of the Emotions in Man and Animals" (third edition) by Charles Darwin, Oxford University Press (1998)

"An exploration of a commonality between ourselves and elephants", by Joyce Poole, "Etica & Animali", vol 9, p 85 (1998)

"Affective Neuroscience" by Jaak Panksepp, Oxford University Press (1998)