A review of the evidence for a biological basis for snake fears in humans.
Evidence From Studies of Non-Human Primates
Three general types of evidence have been presented for our propensity to develop fears of serpent-like creatures and for a biological/evolutionary basis for that propensity. The first type of evidence is derived from a variety of species and merely demonstrates that animals in general demonstrate instances of non-equipotentiality in a variety of contexts (see Domjan & Galef, 1983, for a review). This evidence is of a very general type and merely sets out a wider context for the specific proposition under consideration here. It has no direct bearing on the specific proposal that human beings have a biological predisposition to form fears of serpent-like creatures and, as has been argued by Coleman (2007), is entirely consistent with the writing of those authors who were characterized by Seligman as holding the general process view. Because of the non-contentious nature of these findings and because they have no direct bearing on the specific issue under consideration, they will not be considered here.
The second type of evidence cited by Ohman and Mineka (2001) is the considerable body of evidence that non-human primates selectively attend to and develop negative associations with phylogenically relevant fear stimuli. It seems to be implied that because of our shared evolutionary history with the animal under consideration, it is appropriate to infer that the selective learning observed in such species can be generalized to humans. Much of this evidence comes from the vicarious conditioning procedure developed by Mineka, Davidson, Cook, and Keir (1984) and Cook, Mineka, Wolkenstein, and Laitsch (1985). The development of this paradigm stemmed in part from the observation that wild but not laboratory-reared rhesus monkeys exhibited an intense phobic-like fear of snakes (Joslin, Fletcher, & Emlen, 1964). The studies reported by Mineka et al. (1984) showed that when laboratory-bred monkeys watched wild monkeys acting fearfully toward snakes and non-fearfully toward neutral objects, they acquired fears as intense as the model. Later studies by Cook and Mineka (1989) showed that when the model acted fearfully toward a snake and a flower presented simultaneously, the fear developed only to the snake. Cook and Mineka (1989, 1990) showed that the results were due to superior vicarious conditioning to phylogenically fear-relevant stimuli. Moreover, the excellent animal husbandry procedures at the Wisconsin laboratories ruled out the possibility of accidental ontogenic influences on the outcomes. ohman and Mineka (2001) dealt at length with other criticisms of their conclusions, and it seems likely that rhesus monkeys do indeed respond differently to snake stimuli than to other stimuli. Shibasaki and Kawai (2009) showed that macaque monkeys (Macaca fuscata) also respond differentially to snakes than to control stimuli. It is not our intention to challenge the findings relating to the responses of monkey species to snake. However, what can be debated is the premature application of these findings to the acquisition of fears by humans. The relevance of these findings to humans is based on the notion of a shared evolutionary history. Ohman and Mineka (2001) speculated that the fear may go back as far as our early mammalian past, to a time when small mammals were subject to predation by larger dinosaurs, although it should be noted that others have suggested that this differential responding emanates as an adaptation for the avoidance of snake venom (Isbell, 2006).
If the findings from monkey species are relevant to humans, it follows that they should also be observed in species such as chimpanzees, which are more closely related to human beings. Unfortunately, there is very little relevant recent research on these closely related primates. However, some interesting studies of avoidance reactions by chimpanzees were carried out in the Comparative Psychobiology Laboratory at Yale University in the 1930s. These studies were prompted by an interest in the origins of fears in anthropoid apes and specifically focused on the possible biological basis of such fears. This is interesting because it predated Seligman's paper by 40 years and attests to the longevity of this as a concern in the psychological sciences. The first of these studies, reported by Yerkes and Yerkes (1936), focused specifically on whether fears are hereditary or acquired and, if acquired, whether directly or indirectly through social influence. In one of these studies, the authors observed the reactions of various aged chimpanzees to a badminton shuttlecock, a rubber dog, a rubber tube, a live gopher tortoise, and a live glass snake. Subjects were tested in open-air cage measuring 6 x 4 x 2 meters. Their reactions were rated on a 9-point scale ranging from +4 (no inhibition) to--4 (rushing away from the object with conspicuous erection of the hair). Subjects included captive-born infants and older individuals who had spent much of their lives in captivity but had been born in the wild. The findings were that infants responded with much less fear to all stimuli than did the adults. All age groups responded most positively to the shuttlecock and least positively to the tortoise and the snake. The strongest avoidance response of the infants was toward the tortoise. Both the tortoise and the snake greatly repelled the adults. There is nothing in this study to suggest that snakes produce greater reactions than tortoises, but animate objects produce stronger reactions in all age groups. The avoidance response of laboratory-bred infants was weak to all stimuli. The authors concluded that avoidance responses in chimpanzees were a function of movement and did not generalize to serpent-like characteristics. The lack of responsiveness of the infants and their failure to respond differentially to the snake is not consistent with a theory that affords a special status to serpent-like creatures as fear stimuli, based on their phylogenically relevant threat to the species.
A second study by Haslerud (1938) tested chimpanzees ranging in age from 15 months to 16 years. The stimuli were a shuttlecock, a piece of tubing, a mounted tortoise, a mounted alligator, a mounted garter snake, a kerosene lamp with a picture flame, a red ball (stationary or moving), a kerosene lamp with a live flame, a live tortoise, a live snake, and a live alligator. Stimuli were presented either near (10 cm) or far (90 cm) from the subject. The findings were that the adults did not distinguish between the animate and inanimate objects but responded with equal agitation to all stimuli. The authors concluded that the adults' experience allowed them to impute the possibility of movement and other harmful properties to stationary objects. The infants responded with some fear to all live stimuli but not to stationary ones. Infants showed rapid habituation to all stimuli, whereas there was no difference in the responses of adults to the first and second presentations of stimuli. Overall and in all age groups, the tortoise was the most feared stimulus, with the alligator and the snake being feared somewhat less, fire less still, and a stationary ball least. Considerable individual differences were noted. Overall, these results do not support the view that chimpanzees have a propensity to develop fears toward snakes. There is evidence that movement is an important attribute of objects that cause avoidance and fear in young chimpanzees. However, adults do not seem to respond differentially to moving and motionless objects. Clearly more evidence is required to determine whether higher primates demonstrate differential behavior and associability to serpent-like stimuli, but as things stand, a special status for such stimuli has not been established and movement of any kind seems to be a particularly salient attribute. Until this issue has been resolved, it seems premature to apply to humans findings from the much more remotely related rhesus and macaque monkeys.
Evidence From Experimental Studies of Adult Humans
Another broad category of evidence that has been cited in support of a special status for serpent-like creatures as fear stimuli has come from a large body of studies that have examined a range of reactions by adult humans to fear-relevant stimuli. These reactions have included processing biases and selective visual attention. The studies have used both unselected participants and participants selected because they exhibit a relevant fear. For example, Ohman, Flykt, and Esteves (2001) found that human adults are faster to detect fear targets (snakes and spiders) among a non-fear background (mushrooms and flowers) than non-fear targets against a fear background. Ohman and Mineka (2001) also reported that participants who are fearful of snakes and spiders showed facilitated search for their feared stimulus but did not differ from controls in searching for non-fear stimuli. Tomarken, Mineka, and Cook (1989) used the illusory correlation procedure in which either fear-irrelevant, fear-relevant, or neutral stimuli were paired randomly with shocks, tones, or nothing. Fearful participants were found to overestimate the correlation between fear stimuli and shocks. These are examples of a steady stream of studies in this vein since the publication of Seligman's (1970) landmark article. There have been steady improvements in the rigor of such studies and, as a body of work, it seems pretty sound. There is little basis for disputing the conclusion that human adults, especially snake-fearful ones, behave differently toward images of snakes and similar creatures. However, these studies have no bearing on the issue at hand. The problem is that human adults have not been and could never be subjected to the husbandry regimens found in primate laboratories and, as a consequence, there is a complete confounding of ontogenic and phylogenic influences. For this reason, any difference in the manner in which adult humans react to fear-relevant stimuli can he attributed to cultural influences and other experiential factors. Indeed all of the studies that have used snakes as fear stimuli have been carried out in Western societies. No studies have been reported on participants from societies or subcultures where snakes are tolerated. For example, Hambly (1929) described a number of African societies in which python worship and associations of snakes with positive attributes, such as fecundity, are common. Studies of participants from such cultures would provide interesting comparisons with the studies that have concentrated on participants drawn from Western industrialized societies that have been featured in much of the research to date.
Evidence From Studies of Human Children and Infants
Given the limited relevance of the adult studies to separating ontogenic and phylogenic influences on the origin of snake fears, it is important to turn our attention to research on children. It turns out that there are relatively few studies of this type to consider. An early study by Jones and Jones (1928) presented a large harmless snake to children who ranged in ages from 1 to 10 years and invited them to handle it. The procedure was then repeated with college students. The youngest children (1-2 years) showed no fear, and an older group (2-6 years) was only slightly guarded. In contrast, two thirds of the college students responded with fear, reacting in some cases with barely controlled terror. The most parsimonious interpretation of these observations is that as humans are exposed to the prevailing cultural representations of snakes, they become increasingly wary of them. It is difficult to see the evolutionary advantage of a predisposition to develop a fear of snakes that is only activated long after the child could have learned through experience and instruction that snakes are dangerous and should be avoided. Moreover, a theory that allows for the late emergence of a phylogenic predisposition will not be testable because ontogenic and phylogenic influences would always be confounded.
A more recent study by Waters, Lipp, and Spence (2008) examined the behavior of young children to snake stimuli. They measured visual search times for animal fear stimuli and compared them with search times for control stimuli. Faster location times were obtained for snakes and spiders among mushrooms and flowers than for flowers and mushrooms among snakes and spiders. However, there are a number of problems with this study. There is no account in the Method section of any attempt to ensure that the different types of stimuli were similar in all respects apart from the intended experimental manipulation. A cursory examination of the stimuli provided by the author reveals that the stimuli were very different. The black-and-white reproductions of the stimuli suggest that the fear stimuli were dark against featureless light colored backgrounds, while the non-fear stimuli were plants and mushrooms against mottled backgrounds. There is clearly a much greater contrast of figure and background for the fear stimuli than for the non-fear stimuli, and any difference in detection time could be attributable to the difference. Indeed, similar issues may arise in other experiments that have used pictorial representations of fear and non-fear stimuli. Another issue that calls into question the relevance of the Waters et al. study is the fact that the youngest children were verbally competent 9-year-olds who had been exposed to lengthy, uncontrolled direct and indirect experiences with the fear stimuli.
LoBue and DeLoache (2008) reported studies in which 2-year-old children had to detect pictures of snakes against an array of background distracter stimuli. Latencies on this task were compared with latencies to detect control stimuli against a background of snake stimuli. Nine photographs were presented in each trial in a 3 x 3 array that contained one target stimulus. It was observed that latencies to detect the fear-relevant stimuli were faster than for non-fear control stimuli. The authors were conscious of the need to determine the equivalence of the target stimuli and used a procedure in which a coder, who was blind to the purpose of the research, rated the brightness of the stimuli. The average brightness of the snake and control stimuli was 2.7 on a subjective 5-point scale. However, no attempt was made to ensure equivalence of contrast between the stimuli and their backgrounds. The authors did not provide sample stimuli in the Method section but did provide a picture of the experimental setup in which a child is clearly photographed in the act of locating a flower in an array of snakes. From this photograph, it is apparent that there is a greater contrast between the snakes and their backgrounds than between the flower and its background. Moreover, although it is claimed that the children had little preexperimental exposure to snakes, it is likely that even 2-year-olds in Western culture will have encountered snakes in books and other media.
We will now turn our attention to some very important recent studies of the behavior of very young preverbal children toward fear-relevant stimuli. Studies of this type are important because they offer the potential to separate ontogenic and phylogenic influences on the development of fear. They are also important because from an adaptive point of view, it would seem reasonable to expect a predisposition to avoid phylogenically relevant fear stimuli to be present from a very young age to guide children safely through to early developmental stage, when they can learn from instruction and experience about the dangers in the world. DeLoache and LoBue (2009) set out to examine the behavior toward fear-relevant and fear-irrelevant stimuli of preverbal children (9-10 months old). This involved recording looking durations for two films presented simultaneously, one of snakes moving and another of non-snake animals (giraffe, rhinoceros, polar bear, hippopotamus, elephant, and large bird) moving. In Experiment 1, the children were simply presented simultaneously with 8-s clips of a slithering snake or a moving animal. No differences were observed in the gaze durations for the two clips. In Experiment 2, the procedure was similar. However, on half the trials, the infants were exposed to a happy sounding voice, and on the remaining trials, to a frightened voice. It was observed that a longer time was spent looking at the snake in the presence of the frightened voice than in the presence of the happy voice. However, it should be noted that there was no evidence that the participants spent longer looking at the snake than at the animal in the presence of the frightened voice, and nothing is made of this by the authors. This is worth noting, because all previous studies compared behavior toward snakes and control stimuli in the same condition, whereas this study concentrated on differences in looking at snakes under two different conditions. In Experiment 3, still pictures were used instead of moving images and no differences were noted. The authors concluded that there was something about the characteristic movement of the snake that produced the difference in responding in the two voice conditions. The findings of DeLoache and LoBue are very important because they are purported to be the first demonstration of a separation of ontogenic and phylogenic influences. In passing, it is worth noting that the importance attributed to movement by the authors is not consistent with the original proposition by Ohman and Mineka (2001), who speculated that the special status of snakes dates from a period in which our early mammalian ancestors were subjected to predation by large dinosaurs, which presumably lacked the characteristic movement of modern snakes. This part of the Ohman and Mineka theory is necessary to justify the relevance of the rhesus monkey data, so it cannot be dismissed as a minor detail. This aspect of the findings also calls into question the relevance of previous studies that have used still images.
The first procedural weakness in the DeLoache and LoBue (2009) study that renders the authors' conclusions premature relates to the nature of the control stimuli. It is a curious feature of the experiments that the comparison non-snake animals were some of the largest land mammals on the planet. They included an elephant; a hippopotamus, a giraffe, and a rhinoceros. The snakes were all much smaller. Because the sizes of the projected images were approximately equal, the snake films were close-up images of snakes and the comparison stimuli were films of large animals in the distance. It really is curious that the authors did not choose as comparison stimuli images of similarly sized animals, such as rats and squirrels. It is very possible that the difference observed in the outcome of Experiment 2, which used moving images, and Experiment 3, which used still images, was due to the infants looking at the near object in the presence of the frightened voice. The failure to observe differential responding in Experiment 3 may due to the absence of distance cues in the still images. It is important to note that infants as young as the ones used in this study can differentiate objects of similar retinal image size based on the distance of the objects (Slater, Mattock, & Brown, 1990). So it is quite possible that the results observed in Experiment 2 of the DeLoache and LoBue study can be attributed to a propensity of infants to look at near moving objects in the presence of a frightened voice and not to the serpent-like movement of the stimuli.
A second problem with the study is the manner in which DeLoache and LoBue (2009) chose to report their findings. In reporting the results of Experiment 3, in which still images were used, the authors state that "of most importance, they did not look longer at a still snake than a still animal when they heard a frightened voice" (p. 206). This is true, but it is also true that the participants in Experiment 2 did not look any longer at a moving snake than a moving animal in the presence of a frightened voice. As has been previously stated, in reporting Experiment 2, the authors chose to focus on the difference between snake looking times in the two voice conditions. It is not clear why the authors chose to focus on different comparisons in reporting two very similar experiments. However, the failure to observe a differential preference for looking at either moving or still snakes in comparison to non-snake animals in the presence of either a happy or a frightened voice surely constitutes evidence that there is no predisposition in infants to associate snakes with fear and that the differential responding to snakes observed in adults is a result of ontogenic experiences. Interestingly DeLoache, one of the authors of the paper under consideration, has published an account of some interesting studies of the impact of picture storybook reading on the psychological development of young infants, precisely the type of exposure that may present young children with a negative stereotype of snakes (Simcock & DeLoache, 2008).
LoBue and DeLoache (2011) reported a series of experiments in which they attempted to identify the characteristics of snakes that render them so special. These studies used children ages 3 to 4 years and their parents as participants and used a touch screen method to measure stimulus detection times. This paper is interesting for a number of reasons. First, by using verbal children and their parents as participants, it seems to be assumed that the issue of the evolutionary basis of snake fears has been resolved. These studies were not intended to demonstrate the phylogenic basis of such fears, as they did not use very young infants. In a sense, the authors seemed to imply that the issue of the source of the fear has been resolved and what needed to be established was why snakes have this special status. Second, there was also an implicit acknowledgement in this paper of the limitations of earlier studies. For example, the issue of different backgrounds for snake and non-snake stimuli as a confounding variable was discussed and a decision was made to remove all backgrounds. This decision was sound from a methodological perspective, but it implicitly undermined much of the authors' own earlier research in which backgrounds of different stimuli were not considered or controlled. Finally, the major conclusion of the paper was in itself problematic. One of the major findings of this paper was that a coiled snake was not detected any faster than a coiled wire. Previous studies had used coiled objects as control stimuli to examine the status of snakes (Haslerud, 1938). A failure to observe a difference between the snake and the control stimulus would have been taken as a lack of evidence for the special status of snakes as fear stimuli. Curiously, this finding was welcomed by LoBue and DeLoache as evidence that coiling is the feature that renders snake stimuli special. This conclusion is also problematic for the general theory proposed by Ohman and Mineka (2001). Throughout this paper, the authors cited Ohman and Mineka; however, they seem to be unaware that their conclusion is in direct contradiction with the proposition by Ohman and Mineka that the special status of snakes originates from a period in which our early mammalian ancestors were subjected to predation by large dinosaurs, which lacked the coiling identified in this paper as the feature that affords snakes their special status. In summary, this paper does not address the issue of the source of snake fears, because it involves participants for whom there is a confounding of ontogenic and phylogenic influences; it draws a conclusion that contradicts the view of Ohman and Mineka that snake fears have a very ancient origin and date to the time of dinosaurs.
Rakison (2009) reported a study that used a visual habituation paradigm, in which 11-month-old female infants were shown to associate negative facial emotions with fear-relevant stimuli, including images of snakes and spiders. A similar effect was not observed for male infants. A number of issues are worth considering in relation to these findings. The first is a general issue that has been raised in relation to other studies considered: There is no account of a systematic attempt to ensure that the stimuli used were equivalent in all respects, apart from the intended manipulation. Second, the gender difference reported here is inconsistent with most other studies of this type. For example, the study that most resembles the visual habituation paradigm used in the Rakison study is the vicarious conditioning paradigm used by Mineka et al. (1984). However, in this and related studies, no gender differences were reported for rhesus monkeys. The biological account assumes that the shared evolutionary history of primate species is a source of preparedness of certain fears. This being the case, it is to be expected that there should be a continuity and consistency of findings from different species. The presence of a gender effect in some but not all studies poses problems for the theory. In passing, it may be noted that the findings of the Rakison study are also inconsistent with those of DeLoache and LoBue (2008; LoBue & DeLoache, 2009), where no gender effect was observed.
A final problem with the Rakison (2009) study, which also applies to the bulk of recent experimental studies of responses of humans to fear-relevant stimuli, relates to the narrow range of comparison stimuli used. Responses of infants to snakes and spiders were compared to their responses to flowers and mushrooms. For some unexplained reason, flowers and mushrooms have featured in many of the experimental studies of snake phobias in the literature. Other comparison stimuli in the recent literature have included images of large land animals. The narrow range of stimuli used is problematic because all that can be deduced from such comparisons is that the participants respond differently to snakes than to the particular comparison stimuli. It cannot be concluded from such comparisons that snakes have a special status as fear stimuli because a host of other potential comparison stimuli have not been assessed. The approach of these experimental investigations contrasts sharply with the approach of fear surveys that originally identified the high incidence of snake phobias in the population. For example, an early study by Means (1936) surveyed how more than 1,000 female college students rated 490 stimuli, one of which was snakes. Indeed, even the early experimental study of snake fears in chimpanzees (Haslerud, 1938; Yerkes & Yerkes, 1936) compared subjects' responses to snakes with their responses to a much wider range of stimuli than has become the norm in recent investigations of the biological basis of snake fears. To look at this issue another way, imagine an experiment in which infants were shown to respond in a consistently different way to moving pictures of clouds than to moving pictures of tractors. Such a result would not justify the conclusion that clouds have a special significance derived from the evolutionary history of the species. Many other potential explanations would have to be excluded and many additional comparison stimuli would have to be made before such an explanation could be entertained. The same applies to the findings of all experimental investigations of the responses of infants to serpent-like creatures. As things stand, all we can conclude is that some infants respond differently to some pictures of snakes than to some pictures of flowers, mushrooms, and large land animals. However, we cannot say with any certainty that it is the serpent-like quality of the stimuli that produces the difference and that this effect has its roots in the evolutionary history of the species because the influences of distance cues, stimulus contrast, and a host of other possible confounding variables have not been ruled out.
The prevalence of snake fears in Western culture has been known about for a long time. Means (1936) found that snakes were the most common fear and had the highest fear rating among young college women in the United States: cancer was second, death of a loved one third, death by burning fourth, and hulls fifth. The high frequency of snake fears is a common observation, although a more recent study found that snake fears were only the third most common fear (Seim & Spates, 2010). The perception of snakes in Western culture and their position as commonly feared stimuli is not disputed here. The nonrandom distribution of snake fears is something that requires explanation. The most widely accepted explanation seems to be that our evolutionary history has prepared us to fear snakes. We seem to have latched on quite early to this explanation and interest in it predates Seligman's (1970) landmark paper. This position has stifled investigations into alternative explanations. Much of the research since the publication of Seligman's paper has been on how people and animals respond to the presentation of potential threat stimuli. Remarkably little attention has been given to how experiences with snakes affect fears. We are aware of many potential ontogenic experiences (e.g., latent inhibition, reading, listening, vicarious experiences, and direct experience) that could influence the distribution of fears, but these have received little attention in the context of snake fears since we decided that this fear is best understood in terms of the presumed experiences of our very distant ancestors. In this paper, the evidence for a phylogenic explanation for the high incidence of snake fears was considered. The general evidence from investigations of adult fears has no specific bearing on the issue, as ontogenic and phylogenic explanations are confounded in such studies. In a sense, these studies provide a richer description of the issue to be explained by elaborating on the nature of the fear. The rhesus monkey studies are interesting, but their relevance is questionable in the context of the chimpanzee studies. At best, it is premature to apply these findings to the human context. The studies of very young children are promising but far from conclusive; all have some limitations. If we wish to compare the effects on behavior of different stimuli, we need to ensure that those stimuli differ only in terms of the intended attribute and that they are equivalent in all other respects. In addition, it is crucial that the response to snakes is compared with responses to a wide range of comparison stimuli. It is acknowledged that this is hard to achieve, but until it is achieved, we must be very circumspect about our inferences. The view that snake fears are of biological origin is widely held and frequently asserted. It is only very recently that the type of investigations necessary to support this conclusion have been carried out. The results of those studies have been far from conclusive. While in the field of psychology it may not be the case that a lie repeated often enough becomes the truth, it seems to be the case that an unproven assertion reported often enough is eventually widely accepted.
From a clinical perspective, snake fears are common but rarely lead to impairment. If they do, they respond well to treatment. However, the issue of snake fears and the source of those fears have received considerable attention in the literature. This may be in part because such fears are easy to study under laboratory conditions and may provide a useful laboratory model for fears in general. However, the assumption that such fears are of biological origin has achieved almost iconic status and is used frequently in textbooks and other accounts to dismiss behavioral accounts of clinical phenomena. For example, in a widely used textbook on abnormal psychology, Seligman and Rosenhan (1998) concluded that "the selectivity and irrationality of phobias suggest that phobias are not instances of ordinary classical conditioning" (p. 130). Dellarosa Cummins and Cummins (1999) also used this example to dismiss learning theories. In presenting evidence that some associations are learned more readily than others, these authors first cited the propensity of humans and other animals to acquire fear responses to animals that posed a threat to our ancestors. Coleman (2007) made the case that the existence of evidence for biological preparedness in general does not pose a problem for the general process perspective. It is also the case that there is no conclusive evidence for a biological preparedness account of snake phobias that poses problems for a view that phobias are learned.
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Correspondence concerning this article should be addressed to Kevin Tierney, School of Psychology, Trinity College, Dublin University, Dublin 2, Ireland; E-mail: email@example.com
Kevin J. Tierney and Maeve K. Connolly
Trinity College Dublin
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|Author:||Tierney, Kevin J.; Connolly, Maeve K.|
|Publication:||The Psychological Record|
|Date:||Sep 22, 2013|
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