Close
Here and now Near horizons Far horizons Q&A Pioneers Videos
Close
Search

42Evolution

Near Horizons

Feeling the fear: the ecology of our most basic emotion

Our eyesight is adapted to recognise certain shapes and patterns, particularly those similar to the elongate bodies and scaly skin of snakes.  Some researchers suggest this stems from an ancient mechanism in our neurology that enabled our ancestors to be particularly effective at recognising snakes.  This implies that like other higher primates today, our ancestors needed to be particularly wary of these lithe predators.
   
This visual acuity for patterns also applies to faces.  In fact we can see snakes and faces in almost anything…  
(Image: Wikimedia commons)

Our eyesight is adapted to recognise certain shapes and patterns, particularly those similar to the elongate bodies and scaly skin of snakes. Some researchers suggest this stems from an ancient mechanism in our neurology that enabled our ancestors to be particularly effective at recognising snakes. This implies that like other higher primates today, our ancestors needed to be particularly wary of these lithe predators. This visual acuity for patterns also applies to faces. In fact we can see snakes and faces in almost anything… (Image: Wikimedia commons)

At dusk by the shore, a shadow catches your eye and you ‘freeze’…  As your body stiffens, your senses switch to high alert…

The hairs on your skin stand on end, your heart hammers, your breath comes in gasps.  You are ready to run away or to attack; you will do whatever it takes to survive.

Then you register that the odd shape is just a dead branch… 

You exhale, feeling your heart slowing down… 


Fear acts fast.

It brings us ‘to our senses’, changing our body state and readying us to act.

All this happens before our conscious mind has taken in what has just happened.  It is not until a split second later that our higher brain circuits make an informed assessment of the situation.

vidence suggests that the need to understand the signs of emotion in the faces of others, along with the detection of predators such as snakes, spiders and large predatory cats, has influenced the evolution of our vision and that of our close primate relatives.   This child’s facial expression communicates alarm; we read the cues of enlarged eyes and flared nostrils as indicating a fearful emotional response.  Both of these actions serve to increase the sensory information available.   (Image: Wikimedia commons)

vidence suggests that the need to understand the signs of emotion in the faces of others, along with the detection of predators such as snakes, spiders and large predatory cats, has influenced the evolution of our visio... moren and that of our close primate relatives. This child’s facial expression communicates alarm; we read the cues of enlarged eyes and flared nostrils as indicating a fearful emotional response. Both of these actions serve to increase the sensory information available. (Image: Wikimedia commons)

This emotion is a sensory-response reflex.  It shifts our body’s physiological state whilst capturing our attention and focussing us on the information we need to evaluate in order to survive.  When startled, other mammals make near-identical physiological and action-based responses.

This reaction is however much more widespread.  All vertebrates, invertebrates, arguably plants too and even single celled organisms respond to direct threats with changes in their body chemistry and resulting ‘behaviour’.

These changes alter the body’s responses, and also present a signal to others, influencing how they react.  The more complex the organism, the more elaborate these cues become.

Amoebae, for instance, perceive chemical stress signals from their neighbours.  Plants under attack from infections or insects release volatile compounds that activate both their own defence responses and those of other plants nearby.  Animals and birds are timid and cautious in situations where others from their group have encountered predator attack.

These tracks in the snow show where a bird has been caught by a predator, probably a grey wolf (Canis lupus).  Sudden stresses such as this swift capture produce short term responses in brain neural circuits and hormonal shifts in the body.  Longer term stresses produce lasting changes in the autonomic nervous system, altering the sensitivity of the emotion-associated neural circuits. Vertebrates from zebrafish to apes, when living under prolonged fear stress, show symptoms which appear equivalent to helplessness and depression in humans.   (Image: Wikimedia commons)

These tracks in the snow show where a bird has been caught by a predator, probably a grey wolf (Canis lupus). Sudden stresses such as this swift capture produce short term responses in brain neural circuits and hormonal... more shifts in the body. Longer term stresses produce lasting changes in the autonomic nervous system, altering the sensitivity of the emotion-associated neural circuits. Vertebrates from zebrafish to apes, when living under prolonged fear stress, show symptoms which appear equivalent to helplessness and depression in humans. (Image: Wikimedia commons)

 

Charles Darwin considered that many animals show simple emotional responses including aggression, fear and disgust.  Today, some researchers define fear as an emotion, whilst others suggest that animal fear is simply the ‘activation of neurological survival circuits’.

Fear drives evolution because it triggers selectable behavioural changes.  The way an organism behaves in response to a threat strongly influences its survival.  We respond much as other animals do to a sudden threat, with an involuntary shift in our physiology and attention.

This common response even occurs at the biochemical level.  The signals our nerve relays use to pass messages between cells (neurotransmitters) also act as signals between the cells of plants, fungi, single celled life forms and even bacteria.  We share our biochemical responses to fear and other emotions with all other living cells.

What other animals do not share is our mental concept of fear.  Our thoughts carry meaning, and deliver us a highly sophisticated experience of even the simplest emotions.  Moreover, we live in an ‘ecology of ideas’ where our internal thoughts as well as our external circumstances bring us experiences which affect our emotional state.  We can be startled by real threats, things that look like threats, things that look threatening, and even the thought of things that may never happen…  For instance few of us have been attacked by snakes or terrorists, although many of us fear them.

So whilst our physiological responses to fear are similar to those of other mammals, the way we understand that fear, and the way we behave as a result, is certainly different.  This raises the question of what has influenced the evolution of these distinctively human responses.

What selectable advantages does fear bring us?  Are animal fears anything like ours?  And what are we really scared of?

At 3:25pm local time, an Azerbaijani Army soldier scans the water of Qadisiyah Lake.  Monitoring from this observation post and others along both the river and the lake side of Hadithah Dam in Iraq, is one of the measures used to guard against terrorist threats from approaching watercraft.   (Image: Wikimedia commons)

At 3:25pm local time, an Azerbaijani Army soldier scans the water of Qadisiyah Lake. Monitoring from this observation post and others along both the river and the lake side of Hadithah Dam in Iraq, is one of the measure... mores used to guard against terrorist threats from approaching watercraft. (Image: Wikimedia commons)

What is ‘fear’?

Fear is a bodily ‘condition’ of arousal in our autonomic nervous system.  In this physiological state our senses are fully open to information, bringing our awareness to the present moment.  The changes in our body are reported back to the brain by the vagus nerve, making us aware of how we ‘feel’.

Our generalised term ‘fear’ in practice describes a spectrum of behaviours from ‘freezing’ (fear induced immobilisation) to ‘fight or flight’.  The fear responses of mammals and birds are learned from direct experience as well as through mimicking the habits of their social group.  This can result in highly individualised responses. Such actions may seem more like personality traits than neural reflexes or ‘automatic’ behaviours.

Ring-tailed Coati (Nasua nasua) engaged in an aggression display; Lüneburg Heath wildlife park, Germany.   (Image: Wikimedia commons)

Ring-tailed Coati (Nasua nasua) engaged in an aggression display; Lüneburg Heath wildlife park, Germany.
(Image: Wikimedia commons)

 

What is true for all organisms, including free-living single cells, is that fear enables them to quickly process the information available and so respond to their circumstances.  The resulting ‘adaptive behaviours’ can take many forms.  Some of these are easy to anticipate; different organisms may have similar strategic responses to an equivalent type of threat.  In contrast, in other circumstances, the same individual may react to a familiar threat in a completely different way.

Encountering a predator at close quarters may prompt an animal to flee or launch a defensive attack, but if further away may instead hide or ‘freeze’ to avoid detection.  Some animals vocalise when alarmed.  Others nearby may mimic these responses; bird chicks respond immediately to adult alarm calls, as do infant primates, even without being aware of the danger that triggers them.

Indirect fears are similarly ‘contagious’. Rats in contact with other rats previously given electric shock treatments pick up their stressed emotional state and show a similar neural activation in their amygdala; this is the brain region that processes learned fear responses.  Injured zebrafish release chemicals detectable by other fish, causing them to become agitated and to swim faster.

Baby Asian elephant (Elephas maximus) making a vocal call.   Juvenile mammals of all kinds make distinctive distress calls, often when unexpectedly separated from their mothers.   (Image: Wikimedia commons)

Baby Asian elephant (Elephas maximus) making a vocal call.
Juvenile mammals of all kinds make distinctive distress calls, often when unexpectedly separated from their mothers.
(Image: Wikimedia commons)

A specific form of fear is provoked in juvenile mammals upon becoming separated from their mother.  This involves making high pitched vocal calls.  These sounds of ‘separation anxiety’ or ‘panic’ response provoke their parents and sometimes also other adults to respond.  In highly social animals such as elephants, any adult in the herd will aid the distressed infant.

We usually think of ‘behaviour’ as the easily observable movements of living things.  Fear, however, can also be understood as a ‘cellular state’, applying to all cells in an organism.

Free-living cells, as well as those in a multicellular body, produce chemical signals when stressed.  These cues act as a sort of ‘chemical barometer’, setting an overall baseline state for the organism anywhere on a scale from deep calm to high alert.

Traumatised animals gain heightened direct fear responses due to an increased sensitivity of their nerve cells to stress cues.  Persistent threats cause fear-activated neural circuits to become more sensitive, and produce more signal ‘receptors’.  Greater numbers of these protein ‘antennae’ at the junctions between nerve cells (the synapses) serve to strengthen the signal they receive and relay.  This makes it easier for an external event to ‘sound the alarm’ in a stressed animal.

Conversely, prolonged calm conditions promote relaxation which lowers the nerve cell sensitivity, making the animal more resilient to intermittent stress.

Chimpanzees (Pan troglodytes) in Uganda. These animals, like other of our close primate relatives, use mutual grooming to bond their tribe.  Affectionate touch is vital for these animals’ emotional wellbeing.   In mammals, affectionate touch and body warmth stimulates the vagus nerve to release oxytocin.  This calms the body, particularly the heart and gut, reducing their fear response and increasing their perceived experience of safety and pleasure.   (Image: Wikimedia commons)

Chimpanzees (Pan troglodytes) in Uganda. These animals, like other of our close primate relatives, use mutual grooming to bond their tribe. Affectionate touch is vital for these animals’ emotional wellbeing. In mammal... mores, affectionate touch and body warmth stimulates the vagus nerve to release oxytocin. This calms the body, particularly the heart and gut, reducing their fear response and increasing their perceived experience of safety and pleasure. (Image: Wikimedia commons)

What are the advantages of being scared?

Fear turns information into action.  Whilst these behaviours seek to keep the individual alive, social animals respond collectively to their circumstances.  The way in which a group of animals makes its decisions is an advantage only if it increases the success of the population.

In evolutionary terms fear brings two ‘adaptive responses’ that impact group survival.

 (a) Fear is a teacher

Most fear-associated responses are learned from others.  This is true for all animals, not just social mammals and birds.  For example, crickets copy the spider avoidance strategies of older and more experienced individuals. Marine and freshwater snails avoid foraging in situations where (they or) other snails have unexpectedly encountered a predator, at times remembering for days afterwards.

Mussels (Mytilus edulis) if startled, snap their shells closed.  They also deliberately ‘hide’, keeping their shells closed for longer under conditions of heavy predation by dog whelks (Nucella lapillus).  A reduction in the time an individual spends feeding is copied by others nearby.  This cut in food intake slows their growth and that of the whole population.   (Image: Wikimedia commons)

Blue mussels (Mytilus edulis) if startled, snap their shells closed. They also deliberately ‘hide’, keeping their shells closed for longer under conditions of heavy predation by dog whelks (Nucella lapillus). A redu... morection in the time an individual spends feeding is copied by others nearby. This cut in food intake slows their growth and that of the whole population. (Image: Wikimedia commons)

Animals from fish to flies all undergo fear-associated learning and have some form of ‘memory’.  Juvenile mammals imprint the responses of other adults, so assimilating the collective experience of their social group.  This aligns their behaviour strategies with successful animals; members of their ‘tribe’ are the survivors.  These imprinted responses are then modulated as the individual gains further experience.

Learning is vital to our survival.  Our brain’s limbic system, in particular the amygdala, allows us to learn from experiences and to evaluate new situations against those stored as memories.  Animals with a damaged amygdala fail to respond to cues warning them of danger.

Rats, birds and lizards and even fish also have a simplified limbic system with brain regions performing amygdala-like functions.  This mechanism makes an animal’s learning adaptable, and tailors the magnitude of their response to the perceived level of danger.

Brain section diagram showing the position of the amygdala (in red).  These twin structures are shared between brain hemispheres.   The mammalian amygdala has many neural foci interconnecting with other associated brain regions including those associated with memory (the hippocampus) and anxiety (the stria terminalis).  Within the limbic system, incoming sensory information is relayed by the thalamus in two directions.  Un-processed information passes through the amygdala to the hippocampus, where it is compared against memories of prior experiences.   At the same time, the same sensory information is processed the higher brain regions (the sensory cortex) and from there to the hippocampus.  The combined results of this higher and lower brain processing passes back between the amygdala and the hypothalamus, generating an ‘output’, which shifts the body’s physiology in line with the degree and type of response.   (Image: Wikimedia commons)

Brain section diagram showing the position of the amygdala (in red). These twin structures are shared between brain hemispheres. The mammalian amygdala has many neural foci interconnecting with other associated brain re... moregions including those associated with memory (the hippocampus) and anxiety (the stria terminalis). Within the limbic system, incoming sensory information is relayed by the thalamus in two directions. Un-processed information passes through the amygdala to the hippocampus, where it is compared against memories of prior experiences. At the same time, the same sensory information is processed the higher brain regions (the sensory cortex) and from there to the hippocampus. The combined results of this higher and lower brain processing passes back between the amygdala and the hypothalamus, generating an ‘output’, which shifts the body’s physiology in line with the degree and type of response. (Image: Wikimedia commons)

(b) Fear stabilises the ecosystem

The fear-triggered behavioural strategies of some animals may be ecologically ‘optimised’.  For instance, marine snails ‘hide’ from predatory shore crabs.  This reduces their time spent foraging.  Similarly, mule deer reduce their grazing time when they hide from mountain lions.  In both cases, fear is altering the rate at which these prey consume their food resources, and also reduces the resource consumption of their predators.

Joel Brown and co-workers have studied this phenomenon in lions and their prey.  The time spent ‘hiding’ changes according to the extent of the perceived threat; small increases in predator numbers produce an exponential increase in prey avoidance behaviour.  Conversely a small decrease in predator numbers result in much bolder prey, putting them at substantially greater risk.

This is curious: the reduction in perceived risk here is out of proportion to the chances of predation, suggesting that this mechanism works against protecting the individual.  So what’s the explanation?

Lions kill only a tiny fraction of their potential prey. The flexibility in the fear response of the prey prevents them from being over-exploited by their predators.  This also regulates the prey’s resource use, making them less likely to overgraze their habitat.

A pride of lions (Panthera leo) demolishing the carcass of a zebra. George Schaller’s classic studies of lion populations on the Serengeti concluded that these predators do not directly regulate the numbers of wildebeest, zebra and gazelles.  Instead, their presence in the environment modifies the time they spend hiding from predators.   When lion numbers are low, the prey’s resulting boldness makes it much easier for these predators to feed and so recover their population numbers.   (Image: Wikimedia commons)

A pride of lions (Panthera leo) demolishing the carcass of a zebra. George Schaller’s classic studies of lion populations on the Serengeti concluded that these predators do not directly regulate the numbers of wildebe... moreest, zebra and gazelles. Instead, their presence in the environment modifies the time they spend hiding from predators. When lion numbers are low, the prey’s resulting boldness makes it much easier for these predators to feed and so recover their population numbers. (Image: Wikimedia commons)

 

Erol Akcay and Jeremy Van Cleve have shown that in the case of mammals, although reduction in fear puts individuals at greater risk, the resulting flexibility in their responses has a stabilising effect on the population and consequently the whole ecosystem.  This implies that fear has evolved to optimise the survival of the group.

Are human fears also adaptations?

We share some fear triggers with our close primate relatives.  The main risks to chimpanzee survival come from snakes and other predators, and also from other, aggressive males within their tribe.  Today’s lifestyle has the consequence that most of us never encounter snakes, yet fears and phobias of snakes are widespread.

Our vision is particularly sensitive to moving elongated shapes and to diamond patterns – such as the bodies and diamond-shaped scales of snakes.  Lynne Isbell suggests that our ancestors were bitten and even preyed upon by these reptiles, and their need to detect and avoid these predators selected for our highly pattern-sensitive visual system and neurology.

Our facial expressions change from moment to moment, changing the emotional state we convey.   (Image: Wikimedia commons)

Our facial expressions change from moment to moment, changing the emotional state we convey.
(Image: Wikimedia commons)

As we make eye contact, we easily read fear, happiness, surprise, pleasure and other emotions into the faces of others.  Unconscious reflexes involving our mirror neuron network often trigger us to mimic the facial expressions we see.  At the same time we ‘mirror’ each other’s emotions.

Ralph Adolphs proposes that human facial expressions (‘facial gestures’) may have evolved initially as a means to reveal basic danger cues.  This channel may then later have developed to communicate more elaborate social information.  We read these cues easily today.  Often we are not very aware of others’ facial expressions unless their reaction surprises us, or our emotional information processing system highlights an inconsistency, such as kind gentle words from someone who looks angry.

Whilst the risk of lion or snake attack is a legitimate reason to be wary, for most of us our day-to-day lives are physically safe at least from these threats.  Instead, it is now the contents of our thoughts that trigger most of our fears.  Unlike all other animals, we can be scared merely by thinking of something frightening.  Indeed, it seems that being afraid is what frightens us most of all!

Photograph (1909) of Richard Tjader on the Sotik plains of Kenya, holding the now lifeless head of a lioness that very nearly killed him.  This image is taken from Tjader’s book, ‘The Big Game of Africa’, published in 1910.   We respond emotionally today to things that scare us in much the same way as did our distant ancestors, avoiding lions on the savannah.   (Image: Wikimedia commons)

Photograph (1909) of Richard Tjader on the Sotik plains of Kenya, holding the now lifeless head of a lioness that very nearly killed him. This image is taken from Tjader’s book, ‘The Big Game of Africa’, published... more in 1910. We respond emotionally today to things that scare us in much the same way as did our distant ancestors, avoiding lions on the savannah. (Image: Wikimedia commons)

Can our fear of things that exist only in our thoughts be an evolutionary adaptation?  Emotions in mammals elicit action responses.  When our emotions are triggered by ideas, our ‘action responses’ are also internal, relating us to the consequences of these thoughts.  In this way we ‘try out’ our plans in our imagination and evaluate them before executing them in the ‘real’ world.

There are only two emotions: love and fear. All positive emotions come from love, all negative emotions from fear.  From love flows happiness, contentment, peace, and joy.  From fear comes anger, hate, anxiety and guilt. It’s true that there are only two primary emotions, love and fear.  But it’s more accurate to say that there is only love or fear, for we cannot feel these two emotions together, at exactly the same time.  They’re opposites.  If we’re in fear, we are not in a place of love.  When we’re in a place of love, we cannot be in a place of fear.

[Elizabeth Kübler-Ross; Life Lessons  p.118]

Considering our emotions as ‘information’ (as they are for animals) reveals that each brings a gift.  Happiness and joy tell us when we are safe, and whom we can trust.  Sadness shows us what is really important.  Anger’s strong impulses can be harnessed to motivate our actions, and fear ‘brings us to our senses’, opening us to new information and possibilities.

This mechanism allows us to make plans.  Using fear and other emotions to evaluate the potential risks and benefits of our ideas and intended actions enables us to work creatively.  We have applied this ability to the development of our tools and technologies from stone axe heads through medicines to spacecraft.

Fear keeps us safe in this world of human imagination much as it protected our ancestors from snakes and lions.  ‘Feeling our fears’ enables us to work with them as tools, and even to welcome them as friends.  By adapting their advantages to our needs, we equip ourselves to be powerfully creative, and profoundly human.

 Conclusions

  • ‘Fear’ is a perception processing mechanism which results in physiological responses in the body, and in a predictable set of behaviours, known in mammals and many other vertebrates as ‘fight or flight’.
  • It seems appropriate to classify fear is a basic emotion; perhaps the most basic of emotions. Like other emotions, it processes information, allowing animals an instinctual interpretation of their circumstances.
  • Fear has evolutionary uses. It moderates the behaviour of individuals and populations, adapting an animal’s responses to its circumstances in a flexible way.
  • Fear responses are recognisable in even the simplest of animals. These body responses are overlain by greater complexity and higher degrees of information processing in higher vertebrates.  This is most developed in mammals.
  • We may have initially evolved fear to fear snakes, but our ancestors learned to fear each other more, and latterly it is ourselves that we fear the most…
  • Our imagination alone can provoke us to fear, even in the absence of any directly perceived stimulus. This invites us to explore how our emotional information processing system evolved into a perceptive channel that takes us beyond our current circumstances into a whole new ecological world of ‘ideas’.
  • What makes us human is our ability to choose how we respond to our fears, and to use them as tools to transform ourselves and our world.

 

References
Ackay, E. and Van Cleve, J. (2012)  Behavioral responses in structured populations pave the way to group optimality.  The American Naturalist 179, 257-269.
Adolphs, R. et al. (1995)  Fear and the human amygdala.  Journal of Neuroscience 15, 5879-5891.
Adolphs, R. (2013)  The biology of fear.  Current Biology 23, R79-R93.
Anderson, D.J. and Adolphs, R. (2014)  A framework for studying emotions across species.  Cell 157, 187-200.
Brown, J.S. et al. (1999)  The ecology of fear: optimal foraging, game theory, and trophic interactions.  Journal of Mammalogy 80, 385-399.
Catania, K.C. and Remple, F.E. (2005)  Asymptotic prey profitability drives star-nosed moles to the foraging speed limit.  Nature 433, 519-522.
Cohen, D.H. (1975)  Involvement of the avian amygdala homologue (archistriatum posterior and mediale) in defensively conditioned heart rate change.  Journal of Comparative Neurology 160, 13-35.
Coolen, I. et al. (2005)  Social learning in non-colonial insects?  Current Biology 15, 1931–1935.
Darwin, C. (1872)  The Expression of the Emotions in Man and Animals.  University of Chicago Press.
Davis, M. (1992)  The role of the amygdala in fear and anxiety.  Annual Review of Neuroscience 15, 353-375.
Davis, M. (1992)  The role of the amygdala in fear-potentiated startle: implications for animal models of anxiety.  Trends in Pharmacological Sciences 13, 35-41
Feinstein, J.S. et al. (2011)  The human amygdala and the induction and experience of fear.  Current Biology 21, 34-38.
Fiorito, G. and Scotto, P. (1992)  Observational learning in Octopus vulgarisScience 256, 545–547.
Fossati, P. (2012)  Neural correlates of emotion processing: from emotional to social brain.  European Neuropsychopharmacology 22, S487-S491.
Kittilsen, S. (2013)  Functional aspects of emotions in fish.  Behavioural Processes 100, 153-159.
Kübler-Ross, E. and Kessler, D. (2001)  Life lessons: Two Experts on Death and Dying Teach Us About the Mysteries of Life and Living.   Simon and Schuster.
Lanuza, E. et al. (1998)  Identification of the reptilian basolateral amygdala; an anatomical investigation of the afferents to the posterior dorsal ventricular ridge of the lizard Podarcis hispanicaEuropean Journal of Neuroscience 10, 3517-3534.
LeDoux, J.E. (2012)  Evolution of human emotion: a view through fear.  Progress in Brain Research 195, 431-442.
Marshall-Pescini, S. et al. (2013)  Gaze alternation in dogs and toddlers in an unsolvable task: evidence of an audience effect.  Animal Cognition 16, 933-943.
Martinez Garcia, F. et al. (2002)  The pallial amygdala of amniote vertebrates; evolution of the concept, evolution of the structure.  Brain Research Bulletin 57, 463-469.
Oosterwijk, S. et al. (2012)  States of mind: emotions, body feelings, and thoughts share distributed neural networks.  NeuroImage 62, 2110-2128.
Panksepp, J. (2005)  Affective consciousness: core emotional feelings in animals and humans.  Consciousness and Cognition 14, 30-80.
Panksepp, J. (2011)  Toward a cross-species neuroscientific understanding of the affective mind: do animals have emotional feelings?  American Journal of Primatology 73, 545-561.
Peckarsky, B.L.P.A. et al. (2008)  Revisiting the classics; considering non-comsumptive effects in textbook examples of predator-prey interactions.  Ecology 89, 2416-2425.
Reep, R.L. et al. (2007)  The limbic system in mammalian brain evolution.  Brain, Behavior and Evolution 70, 57-70.
Rovero, F.R.N. et al. (1999)  Cardiac and behavioural response of mussels to risk of predation by dogwhelks.  Animal Behaviour 58, 707-714.
Salzman, C.D. and Fusi, S. (2010)  Emotion, cognition, and mental state representation in amygdala and prefrontal cortex.  Annual Review of Neuroscience 33, 173-202.
Schaller, G.B. (1976)  The Serengeti lion: a study of predator-prey relations.  University of Chicago Press.
Schmahmann, J.D. (2010)  The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy.  Neuropsychology Review 20, 236-260.
Speedie, N. and Gerlai, R. (2008)  Alarm substance induced behavioural response in zebrafish.  Behavioural Brain Research 188, 168-177.
Suboski, M.D. et al. (1993)  Social learning in invertebrates.  Science 259, 1627–1625.
Suboski, M.D. (1994)  Social transmission of stimulus recognition by birds, fish and molluscs. In The Ethological Roots of Culture (R.A. Gardner, ed.).  Kluwer Academic.
Suh, G.S.B. et al. (2004)  A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila.  Nature 431, 854-859.
Suvak, M.K. and Feldman Barrett, L. (2011)  Considering PTSD from the perspective of brain processes: a psychological construction approach.  Journal of Traumatic Stress 24, 3-24.
Trussell, G.C. et al. (2011)  The effects of variable predation risk on foraging and growth: less risk is not necessarily better.  Ecology 92, 1799-1806.
Webster, S.J. and Fiorito, G. (2001)  Socially guided behaviour in non-insect invertebrates.  Animal Cognition 4, 69-79.

Back to top