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Human Perceptual and Phobic Biases For Snakes A Review of The Experimental Evidence
Human Perceptual and Phobic Biases For Snakes A Review of The Experimental Evidence
Marcus Baynes-Rock
To cite this article: Marcus Baynes-Rock (2017) Human Perceptual and Phobic Biases
for Snakes: A Review of the Experimental Evidence, Anthrozoös, 30:1, 5-18, DOI:
10.1080/08927936.2017.1270584
twisting as he strove to wriggle away from where I was due to land. I spread
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Human Perceptual and Phobic Biases for Snakes: A Review of the Experimental Evidence
my feet as far as I could before landing and quickly jumped again in the direction away from that
in which the snake was heading; I landed with my heart racing and turned to catch a glimpse
of the snake, who disappeared into the branches and leaf litter beside the trail.
I have long known that the common tree snakes (Dendrelaphis punctulata) of the mid-
north coast are quite harmless; sometimes they rear up if threatened but they are in fact
non-venomous and at worst can only inflict a minor bite on a human. Yet I had reacted as if
I was in mortal danger, Even after I had recognized the tree snake beneath my feet I still made
a second jump and still felt my heart pounding against my rib cage, in the words of Abbey,
“stung by a fear too ancient and powerful to overcome” (1968, p. 20). Moreover, I should
have recognized the snake as harmless even before I jumped in the air the first time; these
little blue and yellow snakes are unmistakable. But I cannot recall seeing the snake prior to
having jumped up in the air. My earliest recollection of this particular snake is of him writhing
on the ground directly beneath me while I was airborne. Try as I might, I cannot recall seeing
this snake from ground level until after I had landed. Considering my overreaction and my
apparent loss of memory, it would seem as if there is a defect somewhere in my cognitive pro-
cessing. However, I shall demonstrate here that my reaction represents a perfectly functional
human being, at least with respect to reactions to snakes.
extent of envenoming by snakes on humans across the world. The sources—academic pub-
lications; WHO, UN, WB, and FAO databases; key informants—were sufficient to arrive at a
sound minimum but due to data lacking in various countries, far from a certain maximum.
These researchers estimate 1.2–5.5 million people bitten by snakes and envenomed annually,
with 20,000–94,000 of these dying from the bite (Kasturiratne et al., 2008). This demonstrates
a modern selective pressure, but these are largely rural folk, agriculturalists, and pastoralists
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Baynes-Rock
who might not be as vigilant as our pre-agricultural ancestors. What of hunter-gatherers? Con-
sidering the small number of hunter-gatherers studied, there is far less evidence. But they are,
or were, in no way immune from snakebite. Elizabeth Marshall Thomas tells of the plight of a
proficient Ju’/hoan hunter named Short Kwi. While Short Kwi might have been proficient at
tracking and killing game, it seems that he was not so adept at spotting snakes. Short Kwi was
bitten by a puff adder and if not for the intervention of the Marshalls who sent the Ju’/hoan
hunter to have his rotting leg amputated, the venom would have cause his entire body to
wither until he wasted away, leaving his family to fend for themselves (Marshall Thomas, 1959).
Neither is envenoming the only threat posed by serpents to hunter-gatherers. While conduct-
ing fieldwork among the Agta Negritos of the Philippines, Thomas Headland interviewed 120
people, asking them to recall incidents of snake attacks. I say attacks because these were not
defensive bites, these were acts of predation upon Agta by reticulated pythons. Over a 39-year
period, no less than six people were killed and eaten by these massive constrictors (Headland
& Greene, 2011).
Considering the perceived danger of snakes, we take it for granted that they should inspire
fear, but classically the explanation for fear of snakes is that it is learned through cultural trans-
mission (see, e.g., Tierney & Connolly, 2013). This is curious however, as ophidiophobia is far
more common than other more relevant phobias; people do not so readily fear things such as
guns, power outlets, and hammers, which should be much more likely to figure as phobic
stimuli in the modern world (Mineka & Öhman, 2002). This in turn has relevance to conservation
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Human Perceptual and Phobic Biases for Snakes: A Review of the Experimental Evidence
and snakes) and fear-irrelevant (flowers and mushrooms) stimuli. However, as predicted by
Preparedness Theory, fear responses to snakes and spiders were far more resistant to
extinction, even after participants were given certainty that there would be no more shocks
(Öhman, Eriksson, & Olofsson, 1975; Öhman, Erixon, & Löfberg, 1975). Many other experi-
ments were carried out using the conditioning paradigm. Hugdahl (1978) found that a verbal
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threat of shock facilitated acquisition of a fear response to both fear-relevant and fear-irrelevant
stimuli, but again extinction was more resistant in the fear-relevant group.
Öhman, Frederikson, and Hugdahl (1978) measured heart rate responses to phobic and
non-phobic stimuli and found that heart rate increased in response to the phobic stimuli as part
of a defense response. Conversely, heart rate actually decreased in response to the non-
phobic stimuli as part of an orienting response. Hugdahl and Kärker (1981) tested the
evolutionary basis by comparing fear responses to images of snakes with fear responses to
images of modern dangers such as damaged power outlets. Again, resistance to extinction
was greater with the biologically relevant stimuli. Cook, Hodes, and Lang (1986) performed
similar experiments using pictures of snakes and spiders against pictures of weapons, also
finding resistance to extinction in the case of the biologically relevant stimuli.
Öhman and Soares (1994) demonstrated that the bodily fear response in humans acts
independently of conscious awareness. In an experiment where fear responses were condi-
tioned to both fear-relevant and fear-irrelevant stimuli, the researchers found that resistance to
extinction was greater in the case of the fear-relevant stimuli, even when presented for only 30
milliseconds followed by a masking stimulus. Such a duration was too brief for there to be any
conscious perception of the stimulus (Öhman & Soares, 1994).
The conditioning experiments have been subject to some criticism. Bennet-Levy and
Marteau (1984) argued that tactile and auditory cues are integral to animal fears and that
Öhman and associates’ studies were thus limited in this regard. Maltzman and Boyd (1984)
argued that previous results were due to an orienting response, where snakes were “more in-
teresting” (p. 45) than power outlets and that the results reflected this salience. However, they
failed to recognize that Öhman, Frederikson, and Hugdahl (1978) had found the exact oppo-
site of an orienting response in their experiment using heart-rate measurements. They also
failed to question why snakes should be more interesting than damaged power outlets. Daw-
son, Schell, and Tweddle Banis (1986) claimed that previous results were due to an expectancy
bias and that, once that bias was controlled for, there was no difference. These authors also
failed to question why there should be greater expectancy with phobic-stimuli.
Others failed to replicate Öhman’s findings (see, e.g., McNally & Foa, 1986; Merckelbach, van
der Molen, & van den Hout, 1987). However, it has been claimed that this was due to flawed
methodology rather than deficiencies in Preparedness Theory (Mineka & Öhman, 2002). Mc-
Nally (1987) reviewed previous findings and acknowledged that resistance to extinction for pho-
bic stimuli had been demonstrated, but argued that prepared fears need not necessarily be
associated with electric shocks, as had been the case in the majority of experiments. Lovibond,
Siddle, and Bond (1993) argued that results were due to “selective sensitization” (p. 449), where
participants were aware that they would receive a shock and were more anxious about it when
faced with pictures of snakes or spiders. Öhman and Mineka (2001) argued that selective sen-
sitization could not account for all of the effects found in conditioning experiments, especially in
experiments using weapons or power outlets as non-phobic stimuli. Additionally, selective
sensitization was not incompatible with an evolutionary explanation for prepared phobias.
Anthrozoös
In general, the results from Öhman and associates support Preparedness Theory, and it is
tacitly accepted that humans are biologically prepared to expect and respond to evolutionar-
ily relevant threats (Öhman & Mineka, 2001). This has parallels in experiments with lemurs,
macaques, and ground squirrels, where these species react fearfully to snakes even with no
previous experience and/or where populations have not been subject to snake threats for
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thousands of years (Coss & Goldthwaite, 1995; Weiss, Brandl, & Frynta, 2015).
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Human Perceptual and Phobic Biases for Snakes: A Review of the Experimental Evidence
experience (Morris, DeGelder, Weiskrantz, & Dolan, 2001). While G.Y. denied any awareness
of images being presented, he did report that “something happened” during the trials in which
stimuli were presented to his right visual field (Morris et al., 2001).
Here Isbell is specific as to the neural pathways that are integral to sub-cortical snake de-
tection. These are the superior colliculus (SC), the part of the thalamus called the pulvinar, and
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the amygdala. While the amygdala plays a role in learned fears, it is the SC–pulvinar pathway
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that appears to be prepared in primates for visual stimuli that represent snakes (Isbell, 2009).
Van Le et al. (2013) have supported this with neural imaging data from experiments with
Japanese macaques. In these experiments, macaques were seated in a monkey chair in front
of a monitor and shown pictures of snake faces, monkey faces (including fearful), monkey
hands, and geometric shapes. The results showed increased activity in the medial and dorso-
lateral pulvinar that was only evident in response to the pictures of snake faces. This supported
other findings that demonstrate the importance of the pulvinar in recognition and response to
snakes. Importantly the research participants had never been exposed to snakes.
Further research by Almeida, Soares, and Castelo-Branco (2015) has extended these find-
ings to humans. Again using neural imaging to locate and measure brain activity in response to
stimuli, the researchers presented participants with a visual processing task using pictures of
snake faces, true snake shapes, and fake snake shapes (i.e., coiled ropes). They found that
snake shapes elicited higher response levels than snake faces and other shapes, indicating the
importance of overall snake physiology as evolutionarily relevant stimuli. Predictably, the SC–
pulvinar pathway and amygdala showed the strongest responses, suggesting “multiple phylo-
genetic fingerprints” (Almeida et al., 2015, p. 2) in sub-cortical responses to evolutionarily
relevant stimuli. In other words, somewhere among the superior colliculus, pulvinar, and amyg-
dala are templates of snakes; molds that await their filling by real snakes as they appear coiled
at one’s feet. These neural structures, according to Isbell (2009), respond to visual stimuli such
as diamond patterns similar to scales, rows of spots moving against a background, hidden
shapes, rows of spots moving together, and checkerboard patterns. When a signal from the su-
perior colliculus reaches the pulvinar, indicating that one or a combination of these patterns has
been encountered, the V2 and V4 cells of the pulvinar interpret the stimulus as a likely snake
and a signal is sent directly to the amygdala to initiate a fear response, which is only subse-
quently mediated by conscious control. Thus, where humans outwardly react non-fearfully to
snakes (see, e.g., Diamond, 1993; Hood & Williamson, 2008) it is still likely that they experience
a physiological change in line with a pre-conscious fear response to the stimuli.
Based on the premise that evolutionary relevant threats should elicit “pre-attentive … visual at-
tention” (Öhman et al., 2001, p. 466), these researchers constructed an experiment in which
participants were exposed to arrays of nine pictures in a 3 × 3 matrix and asked to identify dis-
crepant pictures within these matrices. As with conditioning experiments, these were pictures
of snakes, spiders, flowers, and mushrooms. In line with the hypothesis, participants identi-
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fied discrepant pictures faster when these were of snakes or spiders, and those who already
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Human Perceptual and Phobic Biases for Snakes: A Review of the Experimental Evidence
had a fear of these were faster at detection. These researchers also varied the set size between
2 × 2 and 3 × 3 matrices and found no effect in the case of fear-relevant stimuli.
The visual search paradigm was taken up by Lipp, Derakshan, Waters, and Logies (2004)
in an experiment in which they attempted to replicate the findings of Öhman et al. (2001). With
only minor changes to the experiment, participants were positioned in front of a monitor and
asked to press a button in a hand-held control box when they perceived the presence of an
image that deviated from the array; for example a snake or spider among flowers or mush-
rooms and vice versa. In fact, some of the images used in this experiment were the same as
those used by Öhman and associates. The results were similar to those of the experiment
they were replicating, although these researchers found an effect of set size on the speed with
which participants detected discrepancies. Moreover, this experiment found no difference in
speed of detection between fearful and non-fearful participants.
In a second experiment, Lipp and associates wanted to test whether it was the fear relevance
of spiders and snakes that captured attention or whether it was that these were simply more in-
teresting than flowers and mushrooms. They introduced pictures of cats and horses into the
matrices of the visual search paradigm. They also had participants rate the “pleasantness” of the
animals using a 7-point Likert scale (Lipp et al., 2004, p. 244). The results showed that pictures
of cats and horses were detected equally as fast as those of spiders and snakes, suggesting that
animals in general were more effective in attention capture. In another experiment, pictures of big
cats and wolves were introduced to see if dangerous animals had an effect on attention capture,
but again it was animals in general that produced the effect. The authors did not regard cats as
“phylogenetically fear relevant” (Lipp et al., 2004, p. 247); however, they failed to acknowledge
the potential for aspects of cat morphology to present as stimuli in the sense of Tinbergen’s red
spots. These were spots painted on wooden paddles that, simply through their resemblance to
the red spots on the beaks of adult herring gulls, elicited feeding behavior in herring gull chicks.
Where visual stimuli are being processed sub-cortically, then the pulvinar might be responding
to morphologies common to both big and small cats, rather than overall size. However, this fails
to explain the faster reaction times for pictures of horses.
The visual search paradigm supplanted conditioning in subsequent snake-recognition ex-
periments. Carlson, Fee, and Reinke (2009) approximated the experiments of Cook et al.
(1986) by presenting participants with a dot probe in which an orienting target was displayed
for 1000ms, followed by the stimulus image sets (snake/mushrooms; gun/mushrooms), fol-
lowed by a 100ms backward mask, followed by a target dot in the position in which a snake,
gun, or mushroom had been presented. The time it took participants to locate the target dot
was used to determine whether backward-masked pictures of snakes and guns modulated
spatial attention. The results suggested that they do, but the pictures were curious. The gun
image was primarily a hand with only an ovoid shape above the index finger betraying the
muzzle of a gun. Sub-cortically, this might as well have been a clenched fist as a pointed gun.
Other visual search tests, primarily those of Vanessa LoBue and Judy DeLoache have
been aimed at determining whether snake detection biases are present in infants. If they are,
Anthrozoös
this supposedly lends credence to Snake Detention Theory. In one study, pictures of frogs
and caterpillars were included in 3 × 3 matrices to test further whether it is snakes or snake-
like animals in general that modulate spatial attention in adults and 3–5-year-old children
(LoBue & DeLoache, 2008). Results showed that both adults and children detected snake
images faster than images of flowers, frogs, and caterpillars among the distractors. Soares and
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colleagues have also used the visual search paradigm with attention and emotion measures.
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Again, pictures of snakes were used against pictures of other stimuli, with the results
suggesting that snake detection is privileged especially where there are many distractors, brief
duration of exposure to stimulus, and high perceptual loads (Soares, 2012; Soares & Esteves,
2013; Soares, Lindström, Esteves, & Öhman, 2014)
Here the obvious question is: what is it specifically, morphologically, about snakes that
causes this bias toward detection of snakes among other visual stimuli? In line with this question,
LoBue and DeLoache (2011) employed the visual search paradigm to test whether such things
as bright colors or snake-specific shapes were crucial. Removal of color from the images had
no effect on faster snake detection, thereby not conforming to SDT, which holds that trichro-
matic vision evolved to better detect snakes. Meanwhile, the researchers found that photo-
graphs of objects with coiled shapes did affect detection speeds regardless of whether these
were snakes or electric cables, suggesting that coiled shape is crucial (although compare
Almeida et al., 2015). Moreover, when uncoiled snakes were presented, these were detected
no faster than flowers. Masataka, Hayakawa, and Kawai (2010) also found that the body po-
sition of snakes was crucial to detection; they found adults and 3–4-year-old children detected
pictures of snakes ready to strike faster than pictures of snakes resting.
Another of the features of snakes that LoBue and DeLoache (2008) hypothesized to be
attention getting was slithering movement. They tested this in a series of experiments using
film (DeLoache & LoBue, 2009). In the first, 7–10-month-old infants were exposed to silent-
film footage of snakes and of exotic, non-snake animals and measured the time the infants
spent looking at the stimuli. There was no significant difference in the time infants looked
at snakes, compared with the other animals. The second experiment was aimed at testing
whether humans had an “innate predisposition to learn to fear snakes” (DeLoache & LoBue,
2009, p. 203). This time infants aged 7–9 months and 16–18 months were shown films of
snakes or exotic animals accompanied by fearful or happy voices. The results showed a
significant tendency in both age groups to associate films of snakes with fearful voices.
This raised a question, which was addressed in experiment 2: what is it about snakes that
leads to associations with fearful stimuli? The experimenters exposed children to
photographs, as opposed to film, of snakes and exotic animals, and this time found no
association with fearful voices. They concluded that movement is key to predisposition
toward fearing snakes.
In comparison to Öhman and Mineka’s (2001) proposal for an evolved fear module that
is evolutionarily prepared to fear snakes, LoBue, Rakison, and DeLoache (2010) proposed
a more conservative view in line with Snake Detection Theory, hypothesizing that humans
possess low-level visual biases for perception of snakes. The reason they give for this is that
in research with infants, a perceptual bias toward snake detection has been found but with-
out a fear association. Thus, they conclude that learning is an essential component of pho-
bic acquisition. This position is at odds with that of Poulton and Menzies (2002a), who
undertook a longitudinal study of individuals in what is known as the Dunedin study. Based
on their findings that those who reported specific fears had less lifetime experience with the
Anthrozoös
feared stimuli, these authors argue for a fourth pathway to phobic acquisition. Alongside
conditioning, observation, and verbal transmission, Poulton and Menzies (2002b) propose
a non-associative model, essentially arguing that we are born fearing snakes in different de-
grees. So rather than learning to fear snakes through normal development, we learn not to
fear them. LoBue and Rakison (2013) argue that the longitudinal studies are problematic
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because they rely heavily on parents’ recall. However, both of these positions are in fact
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Human Perceptual and Phobic Biases for Snakes: A Review of the Experimental Evidence
compatible with a developmental model of preparedness. This would allow for a perceptual
bias as per LoBue, but takes into account developmental stages in which fear of snakes
might emerge in the same way as do animal and stranger fears (Marks, 1987), through a
non-associative pathway.
Conclusion
Here I am not advocating the use of live snakes in experiments. Rather, I am pointing out some
flaws in the assumptions made about human perception and cognition. First is the assump-
tion that these remain ontogenetically uniform with respect to dispositions toward fears and
phobias. This is not the case. Different kinds of phobias emerge at different developmental
stages, and animal fears in particular normally emerge after infancy and fade before adulthood
(Marks, 1987). These in turn are dependent upon experiences with the phobic stimuli. Second
Anthrozoös
is the assumption that conscious perception mirrors unconscious perception. There is exper-
imental evidence to indicate that this is not the case. Hence, experiments aimed at under-
standing pre-cortical cognition need to address exactly how these forms of cognition differ to
that of conscious cognition. Third is that these experiments do not seek to understand fully the
interplay between cognition and consciousness with respect to snakes. Snakes are not always
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encountered fleetingly. For example, people in the snake handling sects of the Appalachians
remove venomous snakes from containers for some members of the congregation to
approach and handle (Hood & Williamson, 2008). What are the mental processes involved in
these associations? The simple fact that they employ snakes is meaningful; kittens would con-
ceivably be less effective. There is something about those serpentine bodies that is inscribed
into our psyches, and in order to understand what it is to be human, we need to understand
what it is to experience snakes, unconsciously, consciously, and in their phenomenological
fullness that draws the full expression of human adaptiveness and its physiological expression.
We cannot do this adequately with images on screens.
Acknowledgements
Thanks to Nick and Sean Atwell for assistance with field research, and two anonymous
reviewers for helpful comments. This work was partly supported by the John Templeton
Foundation under Grant number 57496. The opinions expressed in this publication are those
of the author and do not necessarily reflect the views of the John Templeton Foundation.
Conflicts of Interest
The author reports there are no conflicts of interest.
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