Does women's greater fear of snakes and spiders originate in infancy?

Previous studies with adult humans and nonhuman animals revealed more rapid fear learning for spiders and snakes than for mushrooms and flowers. The current experiments tested whether 11-month-olds show a similar effect in learning associative pairings between facial emotions and fear-relevant and fear-irrelevant stimuli. Consistent with the greater incidence of snake and spider phobias in women, results show that female but not male infants learn rapidly to associate negative facial emotions with fear-relevant stimuli. No difference was found between the sexes for fear-irrelevant stimuli. The results are discussed in relation to fear learning, phobias, and a specialized evolved fear mechanism in humans.     

The Hidden Snake in the Grass: Superior Detection of Snakes in Challenging Attentional Conditions

Snakes have provided a serious threat to primates throughout evolution. Furthermore, bites by venomous snakes still cause significant morbidity and mortality in tropical regions of the world. According to the Snake Detection Theory (SDT Isbell, 2006; 2009), the vital need to detect camouflaged snakes provided strong evolutionary pressure to develop astute perceptual capacity in animals that were potential targets for snake attacks. We performed a series of behavioral tests that assessed snake detection under conditions that may have been critical for survival. We used spiders as the control stimulus because they are also a common object of phobias and rated negatively by the general population, thus commonly lumped together with snakes as “evolutionary fear-relevant”. Across four experiments (N = 205) we demonstrate an advantage in snake detection, which was particularly obvious under visual conditions known to impede detection of a wide array of common stimuli, for example brief stimulus exposures, stimuli presentation in the visual periphery, and stimuli camouflaged in a cluttered environment. Our results demonstrate a striking independence of snake detection from ecological factors that impede the detection of other stimuli, which suggests that, consistent with the SDT, they reflect a specific biological adaptation. Nonetheless, the empirical tests we report are limited to only one aspect of this rich theory, which integrates findings across a wide array of scientific disciplines.     

Human young children as well as adults demonstrate 'superior' rapid snake detection when typical striking posture is displayed by the snake

Humans as well as some nonhuman primates have an evolved predisposition to associate snakes with fear by detecting their presence as fear-relevant stimuli more rapidly than fear-irrelevant ones. In the present experiment, a total of 74 of 3- to 4-year-old children and adults were asked to find a single target black-and-white photo of a snake among an array of eight black-and-white photos of flowers as distracters. As target stimuli, we prepared two groups of snake photos, one in which a typical striking posture was displayed by a snake and the other in which a resting snake was shown. When reaction time to find the snake photo was compared between these two types of the stimuli, its mean value was found to be significantly smaller for the photos of snakes displaying striking posture than for the photos of resting snakes in both the adults and children. These findings suggest the possibility that the human perceptual bias for snakes per se could be differentiated according to the difference of the degree to which their presence acts as a fear-relevant stimulus.     

Aposematic colouration does not explain fear of snakes in humans

Snakes elicit a higher level of fear than other vertebrate animals, yet specific cues responsible for fear of snakes are equivocal. The bright colouration hypothesis suggests that fear responses to snakes are triggered by aposematic colouration, not by snakes per se. We investigated the role of aposematic colouration in fear of snakes in a sample of 10- to 15-year-old Slovak children. Both aposematically and cryptically coloured snakes presented as both colour and black-and-white pictures received higher perceived fear scores than other vertebrates. This suggests that aposematic colouration does not play a crucial role in eliciting fear of snakes. Our results support the snake detection theory suggesting that the human visual system has been influenced by long coexistence between predatory snakes and mammals. As a result, humans have evolved an attentional bias ultimately focused on the correct and rapid detection of these threats.     

Phenotypically plastic responses to predation threat in the mangrove rivulus fish (<Emphasis Type="Italic">Kryptolebias marmoratus</Emphasis>): behavior and morphology

Early life environments have important effects on phenotype development, but it can be difficult to disentangle the relative influences of genotype and environment on phenotypic variation within and among populations. Mangrove rivulus fish (Kryptolebias marmoratus) reproduce by self-fertilization and can generate isogenic lineages, which provides opportunities to resolve how the environment shapes the phenotype independent of genetic variation. Rivulus’ ecology is not well understood, but mangrove water snakes (Nerodia clarkii compressicauda) are thought to be a major predator. To test developmental responses to predator-related cues, four rivulus lineages (two that naturally co-exist with snakes; two that do not) were exposed to one of three treatments for 30 days post-hatching: cues from snakes that were fasted, fed rivulus, or fed heterospecifics. One week after exposure, fear and boldness responses were quantified. Individuals were photographed at 2 and 6 months of age for body size, growth, and body shape analysis. Animals that have historically encountered snakes were more risk averse and had wider heads than animals that historically have not encountered snakes. Rivulus exposed to cues from snakes fed conspecifics or heterospecifics grew faster than those exposed to fasted snake cues. Body shape was more streamlined in animals exposed to cues from snakes fed conspecifics, which may facilitate increased jumping performance as a way to escape aquatic predators. Our results suggest that rivulus exhibit phenotypic plasticity in response to cues associated with predator threat and that historical effects from selection or other evolutionary processes also are important determinants of behavioral and morphological variation.     

Early life environment determines the development of adult phobic‐like fear responses in BALB/cAnN mice

Environmental factors may unleash genetically determined susceptibility to psychopathology. Great effort has been spent in identifying both the genetic basis and environmental sources of exaggerated fear in animal models of anxiety disorders. Here, we show that the origin of inbred mice, probably via subtle differences in breeding and rearing conditions, may have large consequences specifically on acquisition and retention of fear memories, while leaving anxiety‐related behaviours unaffected. These effects could be seen in BALB/cAnN (BALB), but not in C57BL/6N (C57BL/6) mice, thus suggesting their dependency on the genetic background. Increased susceptibility for developing exaggerated fear responses was accompanied by decreased long‐term depression and increased surface trafficking of the AMPA receptor GluR1 subunit at the level of the basolateral amygdala complex. Together, these data raise a novel caveat in the debate about the origins of variation in behavioural studies with experimental animals. Considering that there are currently no animal models which explicitly consider conceptual analogy to the specific gene–environment interactions observed in the aetiology of phobias, our study might suggest a novel approach and direction for further preclinical studies focusing on such aspects of phobic‐like fears.     

Snakes: Interactions with Children with Disabilities and the Elderly—Some Psychological Considerations

ABSTRACT

Over the last three years we have successfully introduced snakes into group activities of children with disabilities, adolescents with behavior problems, and the elderly in nursing homes. This study presents data on the interaction of these groups with four placid and non-poisonous species of snakes of the Boidae and Colubridae families. The primary interactions (PI) included touching, holding, or petting; and the interaction rates during three meetings were recorded. Interaction rates with the children ranged from 50% to 100% and with the elderly from 67% to 86%. In the third encounter 9.5% more elderly agreed to interact with the snakes. When children in the study were offered the choice of a friendly dog, a rabbit, or a snake, 25% to 47% (mean 39%) chose the snake, whereas only 27% and 25% preferred the dog or the rabbit respectively. These results suggest that the affinity and desire of children with disabilities and the elderly to interact with snakes is strong and that this affinity and desire can outweigh cultural stereotypes, widespread fears, and negative attitudes. Many of the negative attitudes, including fear of snakes, are believed to be unconscious and unrelated to conditioned behavior. The psychological significance of the snake as a symbol in the human psyche and culture is discussed in relation to the potential future use of snakes in Animal Assisted Therapy (AAT) with populations that have disabilities.     

Monkey Pulvinar Neurons Fire Differentially to Snake Postures

There is growing evidence from both behavioral and neurophysiological approaches that primates are able to rapidly discriminate visually between snakes and innocuous stimuli. Recent behavioral evidence suggests that primates are also able to discriminate the level of threat posed by snakes, by responding more intensely to a snake model poised to strike than to snake models in coiled or sinusoidal postures (Etting and Isbell 2014). In the present study, we examine the potential for an underlying neurological basis for this ability. Previous research indicated that the pulvinar is highly sensitive to snake images. We thus recorded pulvinar neurons in Japanese macaques (Macaca fuscata) while they viewed photos of snakes in striking and non-striking postures in a delayed non-matching to sample (DNMS) task. Of 821 neurons recorded, 78 visually responsive neurons were tested with the all snake images. We found that pulvinar neurons in the medial and dorsolateral pulvinar responded more strongly to snakes in threat displays poised to strike than snakes in non-threat-displaying postures with no significant difference in response latencies. A multidimensional scaling analysis of the 78 visually responsive neurons indicated that threat-displaying and non-threat-displaying snakes were separated into two different clusters in the first epoch of 50 ms after stimulus onset, suggesting bottom-up visual information processing. These results indicate that pulvinar neurons in primates discriminate between poised to strike from those in non-threat-displaying postures. This neuronal ability likely facilitates behavioral discrimination and has clear adaptive value. Our results are thus consistent with the Snake Detection Theory, which posits that snakes were instrumental in the evolution of primate visual systems.     

Adaptation or preadaptation: why are keelback snakes (<Emphasis Type="Italic">Tropidonophis mairii</Emphasis>) less vulnerable to invasive cane toads (<Emphasis Type="Italic">Bufo marinus</Emphasis>) than are other Australian snakes?

Biological invasions can expose native predators to novel prey which may be less nutritious or detrimental to predators. The introduction and subsequent spread of cane toads (Bufo marinus) through Australia has killed many anuran-eating snakes unable to survive the toad’s toxins. However, one native species, the keelback snake (Tropidonophis mairii), is relatively resistant to toad toxins and remains common in toad-infested areas. Is the keelback’s ability to coexist with toads a function of its ancestral Asian origins, or a consequence of rapid adaptation since cane toads arrived in Australia? And does the snake’s feeding preference for frogs rather than toads reflect an innate or learned behaviour? We compared keelback populations long sympatric with toads with a population that has encountered toads only recently. Unlike toad-vulnerable snake species, sympatry with toads has not affected keelback toxin tolerances or feeding responses: T. mairii from toad-sympatric and toad-naïve populations show a similar sensitivity to toad toxin, and a similar innate preference for frogs rather than toads. Feeding responses of neonatal keelbacks demonstrate that learning plays little or no role in the snake’s aversion to toads. Thus, behavioural aversion to B. marinus as prey, and physiological tolerance to toad toxins are pre-existing innate characteristics of Australian keelbacks rather than adaptations to the cane toad’s invasion of Australia. Such traits were most likely inherited from ancestral keelbacks that adapted to the presence of bufonids in Asia. Our results suggest that the impact of invasive species on native taxa may be strongly influenced by the biogeographic histories of the species involved.     

Fear Conditioning to Subliminal Fear Relevant and Non Fear Relevant Stimuli

A growing body of evidence suggests that conscious visual awareness is not a prerequisite for human fear learning. For instance, humans can learn to be fearful of subliminal fear relevant images – images depicting stimuli thought to have been fear relevant in our evolutionary context, such as snakes, spiders, and angry human faces. Such stimuli could have a privileged status in relation to manipulations used to suppress usually salient images from awareness, possibly due to the existence of a designated sub-cortical ‘fear module’. Here we assess this proposition, and find it wanting. We use binocular masking to suppress awareness of images of snakes and wallabies (particularly cute, non-threatening marsupials). We find that subliminal presentations of both classes of image can induce differential fear conditioning. These data show that learning, as indexed by fear conditioning, is neither contingent on conscious visual awareness nor on subliminal conditional stimuli being fear relevant.     

Rhesus Macaques (Macaca mulatta) Use Posture to Assess Level of Threat From Snakes

Once prey animals have detected predators, they must make decisions about how to respond based on a cost‐benefit analysis of their risk level. The threat sensitivity hypothesis predicts that prey animals match their response to the level of risk, with high‐risk predator encounters eliciting stronger evasive responses than low‐risk encounters. Primates are known prey of snakes, yet they vary their responses toward snakes. We predicted that primates match their response to the threat level from snakes by assessing posture, with striking postures indicating greater risk than coiled postures and coiled postures indicating greater risk than extended sinusoidal postures. We tested this prediction in a series of experimental trials in which captive rhesus macaques (Macaca mulatta) were exposed to snake models in those postures. Results supported the predictions: macaques responded more strongly to a snake model in a striking posture than in a coiled posture and more to a snake model in a coiled posture than to an extended sinusoidal snake model. We also examined responses of macaques to a partially exposed snake model to mimic the condition of incomplete information, as snakes are often occluded by vegetation. The occluded snake model evoked a response comparable to that of the striking snake. These findings support the threat sensitivity hypothesis. Rhesus macaques use the posture of snakes as a cue in threat assessment, responding more intensely as threat increases, and they also behave as if risk is elevated when their information about snakes is incomplete.     

柳州市野生蛇资源调查分析

目的为了解本市野生蛇种类资源状况。方法进行市场调查、询问、采访蛇农、实地考查相结合。结果共收集蛇标本57条,经鉴定共分5科15属26种。结论本市蛇种资源并不丰富,但捕捉现象严重,应加强宣传,提高保护意识。     

Beware the serpent: the advantage of ecologically-relevant stimuli in accessing visual awareness

Snakes and spiders constitute fear-relevant stimuli for humans, as many species have deleterious and even fatal effects. However, snakes provoked an older and thus stronger evolutionary pressure than spiders, shaping the vision of earliest primates toward preferential visual processing, mainly in the most complex perceptual conditions. To the best of our knowledge, no study has yet directly assessed the role of ecologically-relevant stimuli in preferentially accessing visual awareness. Using continuous flash suppression (CFS), the present study assessed the role of evolutionary pressure in gaining a preferential access to visual awareness. For this purpose, we measured the time needed for three types of stimuli - snakes, spiders (matched with snakes for rated fear levels, but for which an influence on humans but not other primates is well grounded) and birds - to break the suppression and enter visual awareness in two different suppression intensity conditions. The results showed that in the less demanding awareness access condition (stimuli presented to the participants' dominant eye) both evolutionarily relevant stimuli (snakes and spiders) showed a faster entry into visual awareness than birds, whereas in the most demanding awareness access condition (stimuli presented to the participants' non-dominant eye) only snakes showed this privileged access. Our data suggest that the privileged unconscious processing of snakes in the most complex perceptual conditions extends to visual awareness, corroborating the proposed influence of snakes in primate visual evolution.     

It takes two: sexual strategies and game theory

David Buss’s Sexual Strategies Theory is one of the major evolutionary psychological research programmes, but, as I try to show in this paper, its theoretical and empirical foundations cannot yet be seen to be fully compelling. This lack of cogency comes about due to Buss’s failure to attend to the interactive nature of his subject matter, which leads him to overlook two classic and well known issues of game theoretic and evolutionary biological analysis. Firstly, Buss pays insufficient attention to the fact that, since mate choice is a cooperative decision, what is adaptive for the two sexes individually is irrelevant to the evolutionary explanation of our sexual strategies; instead, all that matters is what is adaptive given the choices made by the other sex. Secondly, Buss does not pay enough attention to the difference between polymorphic and monomorphic evolutionarily stable states in his attempt to empirically confirm his theory. Because of this, the data he presents and analyses are unable to show that natural selection is the most important element in the explanation of the origins of our sexual strategies. In this way, I try to make clear that, at least as things stand now, Buss has failed to provide compelling grounds for thinking that Sexual Strategies Theory can make a major contribution to human psychology.     

Snake diets and the deep history hypothesis

The structure of animal communities has long been of interest to ecologists. Two different hypotheses have been proposed to explain origins of ecological differences among species within present‐day communities. The competition–predation hypothesis states that species interactions drive the evolution of divergence in resource use and niche characteristics. This hypothesis predicts that ecological traits of coexisting species are independent of phylogeny and result from relatively recent species interactions. The deep history hypothesis suggests that divergences deep in the evolutionary history of organisms resulted in niche preferences that are maintained, for the most part, in species represented in present‐day assemblages. Consequently, ecological traits of coexisting species can be predicted based on phylogeny regardless of the community in which individual species presently reside. In the present study, we test the deep history hypothesis along one niche axis, diet, using snakes as our model clade of organisms. Almost 70% of the variation in snake diets is associated with seven major divergences in snake evolutionary history. We discuss these results in the light of relevant morphological, behavioural, and ecological correlates of dietary shifts in snakes. We also discuss the implications of our results with respect to the deep history hypothesis. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 476–486.     

Cytogenetics of the Javan file snake (Acrochordus javanicus) and the evolution of snake sex chromosomes

Advanced snakes (Caenophidia) are an important group including around 90% of the recent species of snakes. The basal splitting of the clade is still rather controversial, and it is not fully understood when the differentiation of sex chromosomes started in snake evolution. To help resolve these questions, we performed cytogenetic analysis on the Javan file snake, also known as the elephant trunk snake (Acrochordus javanicus) from the family Acrochordidae, which occupies an informative phylogenetic position. For the first time for acrochordids, we identified heteromorphic ZZ/ZW sex chromosomes with a highly heterochromatic W chromosome. These traits are likely synapomorphies of advanced snakes. In contrast to other caenophidian snakes, the Javan file snake lacks an accumulation of Bkm repeats and interstitial telomeric repeats on the W chromosome. This observation supports the sister group relationship between acrochordids and all other caenophidian snakes including the family Xenodermatidae and questions the suggested role of Bkm repeats in the formation of sex heterochromatin in snakes. The revealed partial gene content of the Z chromosome in acrochordids supports the hypothesis that the progressive degeneration of the W chromosome commenced in snakes before the basal split of Caenophidia, albeit its evolutionary rate in file snakes might be slower than in their sister lineage.     

Generalization of predator recognition: Velvet geckos display anti-predator behaviours in response to chemicals from non-dangerous elapid snakes

Many prey species detect chemical cues from predators and modify their behaviours in ways that reduce their risk of predation. Theory predicts that prey should modify their anti-predator responses according to the degree of threat posed by the predator. That is, prey should show the strongest responses to chemicals of highly dangerous prey, but should ignore or respond weakly to chemicals from non-dangerous predators. However, if anti-predator behaviours are not costly, and predators are rarely encountered, prey may exhibit generalised antipredator behaviours to dangerous and non-dangerous predators. In Australia, most elapid snakes eat lizards, and are therefore potentially dangerous to lizard prey. Recently, we found that the nocturnal velvet gecko Oedura lesueurii responds to chemicals from dangerous and non-dangerous elapid snakes, suggesting that it displays gen-eralised anti-predator behaviours to chemicals from elapid snakes. To explore the generality of this result, we videotaped the be-haviour of velvet geckos in the presence of chemical cues from two small elapid snakes that rarely consume geckos: the nocturnal golden-crowned snake Cacophis squamulosus and the diurnal marsh snake Hemiaspis signata. We also videotaped geckos in tri-als involving unsceted cards (controls) and cologne-scented cards (pungency controls). In trials involving Cacophis and Hemi-aspis chemicals, 50% and 63% of geckos spent long time periods (> 3 min) freezing whilst pressed flat against the substrate, re-spectively. Over half the geckos tested exhibited anti-predator behaviours (tail waving, tail vibration, running) in response to Ca-cophis (67%) or Hemiaspis (63%) chemicals. These behaviours were not observed in control or pungency control trials. Our re-sults support the idea that the velvet gecko displays generalised anti-predator responses to chemical cues from elapid snakes. Generalised responses to predator chemicals may be common in prey species that co-occur with multiple, ecologically similar, dangerous predators.     

The Distinct Role of the Amygdala,Superior Colliculus and Pulvinar in Processing of Central and Peripheral Snakes

Introduction

Visual processing of ecologically relevant stimuli involves a central bias for stimuli demanding detailed processing (e.g., faces), whereas peripheral object processing is based on coarse identification. Fast detection of animal shapes holding a significant phylogenetic value, such as snakes, may benefit from peripheral vision. The amygdala together with the pulvinar and the superior colliculus are implicated in an ongoing debate regarding their role in automatic and deliberate spatial processing of threat signals.

Methods

Here we tested twenty healthy participants in an fMRI task, and investigated the role of spatial demands (the main effect of central vs. peripheral vision) in the processing of fear-relevant ecological features. We controlled for stimulus dependence using true or false snakes; snake shapes or snake faces and for task constraints (implicit or explicit). The main idea justifying this double task is that amygdala and superior colliculus are involved in both automatic and controlled processes. Moreover the explicit/implicit instruction in the task with respect to emotion is not necessarily equivalent to explicit vs. implicit in the sense of endogenous vs. exogenous attention, or controlled vs. automatic processes.

Results

We found that stimulus-driven processing led to increased amygdala responses specifically to true snake shapes presented in the centre or in the peripheral left hemifield (right hemisphere). Importantly, the superior colliculus showed significantly biased and explicit central responses to snake-related stimuli. Moreover, the pulvinar, which also contains foveal representations, also showed strong central responses, extending the results of a recent single cell pulvinar study in monkeys. Similar hemispheric specialization was found across structures: increased amygdala responses occurred to true snake shapes presented to the right hemisphere, with this pattern being closely followed by the superior colliculus and the pulvinar.

Conclusion

These results show that subcortical structures containing foveal representations such as the amygdala, pulvinar and superior colliculus play distinct roles in the central and peripheral processing of snake shapes. Our findings suggest multiple phylogenetic fingerprints in the responses of subcortical structures to fear-relevant stimuli.     

Alarm Calls of Marmosets (Callithrix geoffroyi) to Snakes and Perched Raptors

Communication about the presence of predators is an important benefit of group living. Critical information about the nature of danger can be conveyed through referential alarm calls. Raptors pose a significant predatory threat to callitrichid species. Unlike a raptor in flight, a perched raptor cannot attack suddenly at great speed, and it can be monitored from a safe distance. In this sense a perched bird may pose a threat more similar to that of a terrestrial predator such as a snake. Here we compare predatory contexts by addressing these two questions: 1) Do marmosets produce acoustically distinct alarm calls to snake models and perched raptor models? 2) Do the visual responses of the marmosets to the playbacks of perched raptor–elicited calls differ from those given to the playbacks of calls given in response to snakes? We recorded alarm calls from two groups of outdoor-housed Geoffroy’s marmosets (Callithrix geoffroyi) in response to predator models. Later, we played back stimuli created from these recordings to the marmosets and scored their gaze direction. Results show that calls given to models of perched raptors are acoustically distinct from those given to models of snakes. Further, the relative number of upward to downward looks while listening to the playbacks of perched raptor–elicited calls was significantly greater than it was for snake-elicited calls. Reactions to airborne raptors are known to elicit freezing or rapid flight, neither of which occurred in response to our playbacks. Our data suggest a greater complexity in the alarm call repertoire of marmosets than previously demonstrated.     

Gravity and the evolution of cardiopulmonary morphology in snakes

Physiological investigations of snakes have established the importance of heart position and pulmonary structure in contexts of gravity effects on blood circulation. Here we investigate morphological correlates of cardiopulmonary physiology in contexts related to ecology, behavior and evolution. We analyze data for heart position and length of vascular lung in 154 species of snakes that exhibit a broad range of characteristic behaviors and habitat associations. We construct a composite phylogeny for these species, and we codify gravitational stress according to species habitat and behavior. We use conventional regression and phylogenetically independent contrasts to evaluate whether trait diversity is correlated with gravitational habitat related to evolutionary transitions within the composite tree topology. We demonstrate that snake species living in arboreal habitats, or which express strongly climbing behaviors, possess relatively short blood columns between the heart and the head, as well as relatively short vascular lungs, compared to terrestrial species. Aquatic species, which experience little or no gravity stress in water, show the reverse — significantly longer heart-head distance and longer vascular lungs. These phylogenetic differences complement the results of physiological studies and are reflected in multiple habitat transitions during the evolutionary histories of these snake lineages, providing strong evidence that heart-to-head distance and length of vascular lung are co-adaptive cardiopulmonary features of snakes.