Health and the avoidance of macroparasites: a preliminary cross-cultural study

Some evolutionary explanations of cross-cultural differences propose that human personality is caused by pathogen stress. Both xenophobia and ethnocentrism evolved under conditions with high parasite prevalence. Further, inter-individual variation in disgust or fear of parasites is expected to be influenced by human health, where healthy people should express lower disgust sensitivity to parasites. We examined inter-individual variation of children’s fear, disgust and self-perceived danger between two distinct cultures differing in overall pathogen prevalence. We found that children were able to distinguish between disease-relevant and disease-irrelevant groups of invertebrates and that children in regions with high pathogen prevalence expressed greater fear, disgust and self-perceived danger of all animals, irrespective of disease threat. After controlling for confounding factors, better health of children was associated with lower perceived danger of disease-relevant animals. Gender differences were found only in conditions with low pathogen stress. Our results support the idea that cross-cultural differences in human perception of animals are mediated by pathogen threat. Further research is necessary to investigate causal relationship between human health and avoidance of potentially hazardous animals.     

Risk of parasite transmission influences perceived vulnerability to disease and perceived danger of disease-relevant animals

Adaptationist view proposes that emotions were shaped by natural selection and their primary function is to protect humans against predators and/or disease threat. This study examined cross-cultural and inter-personal differences in behavioural immune system measured by disgust, fear and perceived danger in participants from high (Turkey) and low (Slovakia) pathogen prevalence areas. We found that behavioural immune system in Turkish participants was activated more than those of Slovakian participants when exposed to photographs depicting disease-relevant cues, but not when exposed to disease-irrelevant cues. However, participants from Slovakia, where human to human disease transmission is expected to be more prevalent than in Turkey, showed lower aversion in Germ Aversion subscale supporting hypersensitiveness of the behavioural immune system. Having animals at home was less frequent both in Turkey and in participants who perceived higher danger about disease relevant animals. Participants more vulnerable to diseases reported higher incidence of illness last year and considered perceived disease-relevant animals more dangerous than others. Females showed greater fear, disgust and danger about disease-relevant animals than males. Our results further support the finding that cultural and inter-personal differences in human personality are influenced by parasite threat.     

Disgust versus Lust: Exploring the Interactions of Disgust and Fear with Sexual Arousal in Women

Sexual arousal is a motivational state that moves humans toward situations that inherently pose a risk of disease transmission. Disgust is an emotion that adaptively moves humans away from such situations. Incongruent is the fact that sexual activity is elementary to human fitness yet involves strong disgust elicitors. Using an experimental paradigm, we investigated how these two states interact. Women (final N=76) were assigned to one of four conditions: rate disgust stimuli then watch a pornographic clip; watch a pornographic clip then rate disgust stimuli; rate fear stimuli then watch a pornographic clip; or watch a pornographic clip then rate fear stimuli. Women’s genital sexual arousal was measured with vaginal photoplethysmography and their disgust and fear reactions were measured via self-report. We did not find that baseline disgust propensity predicted sexual arousal in women who were exposed to neutral stimuli before erotic content. In the Erotic-before-Disgust condition we did not find that sexual arousal straightforwardly predicted decreased image disgust ratings. However, we did find some evidence that sexual arousal increased self-reported disgust in women with high trait disgust and sexual arousal decreased self-reported disgust in women with low trait disgust. Women who were exposed to disgusting images before erotic content showed significantly less sexual arousal than women in the control condition or women exposed to fear-inducing images before erotic content. In the Disgust-before-Erotic condition the degree of self-reported disgust was negatively correlated with genital sexual arousal. Hence, in the conflict between the ultimate goals of reproduction and disease avoidance, cues of the presence of pathogens significantly reduce the motivation to engage in mating behaviors that, by their nature, entail a risk of pathogen transmission.     

Similar neural activity during fear and disgust in the rat basolateral amygdala

Much research has focused on how the amygdala processes individual affects, yet little is known about how multiple types of positive and negative affects are encoded relative to one another at the single-cell level. In particular, it is unclear whether different negative affects, such as fear and disgust, are encoded more similarly than negative and positive affects, such as fear and pleasure. Here we test the hypothesis that the basolateral nucleus of the amygdala (BLA), a region known to be important for learned fear and other affects, encodes affective valence by comparing neuronal activity in the BLA during a conditioned fear stimulus (fear CS) with activity during intraoral delivery of an aversive fluid that induces a disgust response and a rewarding fluid that induces a hedonic response. Consistent with the hypothesis, neuronal activity during the fear CS and aversive fluid infusion, but not during the fear CS and rewarding fluid infusion, was more similar than expected by chance. We also found that the greater similarity in activity during the fear- and disgust-eliciting stimuli was specific to a subpopulation of cells and a limited window of time. Our results suggest that a subpopulation of BLA neurons encodes affective valence during learned fear, and furthermore, within this subpopulation, different negative affects are encoded more similarly than negative and positive affects in a time-specific manner.     

Spiders are special: fear and disgust evoked by pictures of arthropods

Because all spiders are predators and most subdue their prey with poison, it has been suggested that fear of spiders is an evolutionary adaptation. However, it has not been sufficiently examined whether other arthropods similarly elicit fear or disgust. Our aim was to examine if all arthropods are rated similarly, if only potentially dangerous arthropods (spiders, bees/wasps) elicit comparable responses, or if spiders are rated in a unique way. We presented pictures of arthropods (15 spiders, 15 beetles, 15 bees/wasps, and 15 butterflies/moths) to 76 students who rated each picture for fear, disgust, and how dangerous they thought the animal is. They also categorized each animal into one of the four animal groups. In addition, we assessed the participants' fear of spiders and estimates for trait anxiety. The ratings showed that spiders elicit significantly greater fear and disgust than any other arthropod group, and spiders were rated as more dangerous. Fear and disgust ratings of spider pictures significantly predicted the questionnaire scores for fear of spiders, whereas dangerousness ratings of spiders and ratings of other arthropods do not provide any predictive power. Thus, spider fear is in fact spider specific. Our results demonstrate that potential harmfulness alone cannot explain why spiders are feared so frequently.     

Dissociation between Emotional Remapping of Fear and Disgust in Alexithymia

There is growing evidence that individuals are able to understand others’ emotions because they “embody” them, i.e., re-experience them by activating a representation of the observed emotion within their own body. One way to study emotion embodiment is provided by a multisensory stimulation paradigm called emotional visual remapping of touch (eVRT), in which the degree of embodiment/remapping of emotions is measured as enhanced detection of near-threshold tactile stimuli on one’s own face while viewing different emotional facial expressions. Here, we measured remapping of fear and disgust in participants with low (LA) and high (HA) levels of alexithymia, a personality trait characterized by a difficulty in recognizing emotions. The results showed that fear is remapped in LA but not in HA participants, while disgust is remapped in HA but not in LA participants. To investigate the hypothesis that HA might exhibit increased responses to emotional stimuli producing a heightened physical and visceral sensations, i.e., disgust, in a second experiment we investigated participants’ interoceptive abilities and the link between interoception and emotional modulations of VRT. The results showed that participants’ disgust modulations of VRT correlated with their ability to perceive bodily signals. We suggest that the emotional profile of HA individuals on the eVRT task could be related to their abnormal tendency to be focalized on their internal bodily signals, and to experience emotions in a “physical” way. Finally, we speculated that these results in HA could be due to a enhancement of insular activity during the perception of disgusted faces.     

Disgust sensitivity, obesity stigma, and gender: contamination psychology predicts weight bias for women, not men

Recent research has established a link between disgust sensitivity and stigmatizing reactions to various groups, including obese individuals. However, previous research has overlooked disgust's multiple evolved functions. Here, we investigated whether the link between disgust sensitivity and obesity stigma is specific to pathogen disgust, or whether sexual disgust and moral disgust--two separate functional domains--also relate to negative attitudes toward obese individuals. Additionally, we investigated whether sex differences exist in the manner disgust sensitivity predicts obesity stigma, whether the sexes differ across the subtypes of obesity bias independent of disgust sensitivity, and last, the association between participants' BMI and different subtypes of obesity stigma. In study 1 (N = 92), we established that obesity elicits pathogen, sexual, and moral disgust. In study 2, we investigated the relationship between these types of disgust sensitivity and obesity stigma. Participants (N = 387) reported their level of disgust toward various pathogen, sexual, and moral acts and their attitudes toward obese individuals. For women, but not men, increased pathogen disgust sensitivity predicted more negative attitudes toward obese individuals. Men reported more negative general attitudes toward obese individuals whereas women reported greater fear of becoming obese. The sexes also differed in how their own BMI related to the subtypes of obesity stigma. These findings indicate that pathogen disgust sensitivity plays a role in obesity stigma, specifically for women. Defining the scope of disgust's activation in response to obesity and its relationship with other variables can help identify possible mechanisms for understanding and ultimately alleviating prejudice and discrimination.     

Parasites,info-disruption,and the ecology of fear

There is growing interest in the ecological consequences of fear, as evidenced by the numerous studies on the nonconsumptive, trait-mediated effects of predators. Parasitism, however, has yet to be fully integrated into research on the ecology of fear, despite it having direct negative and often lethal effects on hosts and being the most common life history strategy on the planet. This might at least be partly due to the traditional, but untested, assumption that anti-parasite responses are weak relative to anti-predator responses. To test this hypothesis, we quantified the activity and location responses of Bufo americanus tadpoles to one of six chemical cues: water; cercariae of Echinostoma trivolvis, a trematode which infects and can kill amphibians; a snail releasing E. trivolvis cercariae; an uninfected snail; food; or conspecific alarm chemicals signaling predation. There is also literature encouraging research on the context dependency and pollution-induced disruption of fear responses. Consequently, before quantifying responses to the chemical cues, half of the B. americanus were exposed to the herbicide atrazine (201 μg/l for 4 days), a reported inhibitor of fear responses in fish. Tadpoles were attracted to food, were indifferent to an uninfected snail, avoided alarm chemicals, and exhibited avoidance and elevated activity in response to a snail shedding cercariae and cercariae alone. Atrazine had no detectable effects on B. americanus’ responses to the tested cues despite the use of a higher concentration and longer exposure duration than has been repeatedly shown to inhibit chemical cue detection in fish. The magnitude of anti-parasite and anti-predator responses were qualitatively similar, suggesting that the fear of disease and its ecological consequences could be comparable to that of predation. Consequently, we call for a greater integration of parasites into research on the ecology of fear and trait-mediated indirect effects.     

Quantitative analysis of fiddler crab flock movement: evidence for ‘selfish herd’ behaviour

The selfish herd hypothesis predicts that aggregations form because individuals move towards one another, and that this movement will minimize predation risk as measured by the domain of danger. To test the predictions of the selfish herd hypothesis in the field, we videotaped the movements of sand fiddler crab, Uca pugilator, flocks being attacked by predators. After recording 12 attacks on crabs by shorebird and human attackers, we digitized the video, and determined the positions of crabs before and after being frightened. We estimated the time of panic initiation by the rapid increase in the crabs' velocity. Crab flocks became more cohesive after panic initiation. The frequency distribution of the crabs' domains of danger shifted significantly towards smaller domains after panic initiation. The median domain of danger was significantly lower after panic initiation than beforehand. Two other indices of aggregation also showed statistically significant increases in flock cohesion following panic initiation. We conclude that fiddler crab behaviour is consistent with the selfish herd hypothesis. Therefore, our results support the selfish herd hypothesis as an explanation for gregarious behaviour. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Neural responses to facial and vocal expressions of fear and disgust.

Neuropsychological studies report more impaired responses to facial expressions of fear than disgust in people with amygdala lesions, and vice versa in people with Huntington''s disease. Experiments using functional magnetic resonance imaging (fMRI) have confirmed the role of the amygdala in the response to fearful faces and have implicated the anterior insula in the response to facial expressions of disgust. We used fMRI to extend these studies to the perception of fear and disgust from both facial and vocal expressions. Consistent with neuropsychological findings, both types of fearful stimuli activated the amygdala. Facial expressions of disgust activated the anterior insula and the caudate-putamen; vocal expressions of disgust did not significantly activate either of these regions. All four types of stimuli activated the superior temporal gyrus. Our findings therefore (i) support the differential localization of the neural substrates of fear and disgust; (ii) confirm the involvement of the amygdala in the emotion of fear, whether evoked by facial or vocal expressions; (iii) confirm the involvement of the anterior insula and the striatum in reactions to facial expressions of disgust; and (iv) suggest a possible general role for the perception of emotional expressions for the superior temporal gyrus.     

Multimodal Assessment of Long-Term Memory Recall and Reinstatement in a Combined Cue and Context Fear Conditioning and Extinction Paradigm in Humans

Learning to predict danger via associative learning processes is critical for adaptive behaviour. After successful extinction, persisting fear memories often emerge as returning fear. Investigation of return of fear phenomena, e.g. reinstatement, have only recently began and to date, many critical questions with respect to reinstatement in human populations remain unresolved. Few studies have separated experimental phases in time even though increasing evidence shows that allowing for passage of time (and consolidation) between experimental phases has a major impact on the results. In addition, studies have relied on a single psychophysiological dimension only (SCRs/SCL or FPS) which hampers comparability between different studies that showed both differential or generalized return of fear following a reinstatement manipulation. In 93 participants, we used a multimodal approach (fear-potentiated startle, skin conductance responses, fear ratings to asses fear conditioning (day 1), extinction (day 2) as well as delayed memory recall and reinstatement (day 8) in a paradigm that probed contextual and cued fear intra-individually. Our findings show persistence of conditioning and extinction memory over time and demonstrate that reinstated fear responses were qualitatively different between dependent variables (subjective fear ratings, FPS, SCRs) as well as between cued and contextual CSs. While only the arousal-related measurement (SCRs) showed increasing reactions following reinstatement to the cued CSs, no evidence of reinstatement was observed for the subjective ratings and fear-related measurement (FPS). In contrast, for contextual CSs, reinstatement was evident as differential and generalized reinstatement in fear ratings as well as generally elevated physiological fear (FPS) and arousal (SCRs) related measurements to all contextual CSs (generalized non-differential reinstatement). Returning fear after reinstatement likely depends on a variety of variables (experimental design, dependent measurements) and more systematic investigations with respect to critical determinants of reinstatement in humans are required.     

Disgust: the disease-avoidance emotion and its dysfunctions

This review analyses the accumulating evidence from psychological, psychophysiological, neurobiological and cognitive studies suggesting that the disease-avoidance emotion of disgust is a predominant emotion experienced in a number of psychopathologies. Current evidence suggests that disgust is significantly related to small animal phobias (particularly spider phobia), blood-injection-injury phobia and obsessive-compulsive disorder contamination fears, and these are all disorders that have primary disgust elicitors as a significant component of their psychopathology. Disgust propensity and sensitivity are also significantly associated with measures of a number of other psychopathologies, including eating disorders, sexual dysfunctions, hypochondriasis, height phobia, claustrophobia, separation anxiety, agoraphobia and symptoms of schizophrenia--even though many of these psychopathologies do not share the disease-avoidance functionality that characterizes disgust. There is accumulating evidence that disgust does represent an important vulnerability factor for many of these psychopathologies, but when disgust-relevant psychopathologies do meet the criteria required for clinical diagnosis, they are characterized by significant levels of both disgust and fear/anxiety. Finally, it has been argued that disgust may also facilitate anxiety and distress across a broad range of psychopathologies through its involvement in more complex human emotions such as shame and guilt, and through its effect as a negative affect emotion generating threat-interpretation biases.     

Dynamics of visual information integration in the brain for categorizing facial expressions

A key to understanding visual cognition is to determine when, how, and with what information the human brain distinguishes between visual categories. So far, the dynamics of information processing for categorization of visual stimuli has not been elucidated. By using an ecologically important categorization task (seven expressions of emotion), we demonstrate, in three human observers, that an early brain event (the N170 Event Related Potential, occurring 170 ms after stimulus onset) integrates visual information specific to each expression, according to a pattern. Specifically, starting 50 ms prior to the ERP peak, facial information tends to be integrated from the eyes downward in the face. This integration stops, and the ERP peaks, when the information diagnostic for judging a particular expression has been integrated (e.g., the eyes in fear, the corners of the nose in disgust, or the mouth in happiness). Consequently, the duration of information integration from the eyes down determines the latency of the N170 for each expression (e.g., with "fear" being faster than "disgust," itself faster than "happy"). For the first time in visual categorization, we relate the dynamics of an important brain event to the dynamics of a precise information-processing function.     

Human handling and presentation of a novel object evoke independent dimensions of fear in Japanese quail

Fear is a concept comprising several dimensions, but the nature of these dimensions and the relationships between them remain elusive. To investigate these dimensions in birds, we have used two genetic lines of quail divergently selected on tonic immobility duration, a behavioural index of fear. These two lines differ in their behavioural response to some, but not all, fear-inducing situations. In the present study, we investigated the contribution of human intervention in the differentiation between the two lines. To do this, fear responses towards a novel object were compared between lines in three conditions: (1) in the home cage without any human intervention, (2) in the home cage after human handling and (3) after placement in a novel environment by human handling. Fear behaviour differed between lines after human handling, with or without placement in a novel environment, but presentation of a novel object in the home cage without any human intervention induced similar fear responses in the two lines of quail. These results lead us to suggest that in quail, human intervention evokes a dimension of fear that differs from that evoked by sudden presentation of a novel object, in that these two dimensions may be selected independently.     

Fear generalization and behavioral responses to multiple dangers

Animals often exhibit consistent-individual differences (CIDs) in boldness/fearfulness, typically studied in the context of predation risk. We focus here on fear generalization, where fear of one danger (e.g., predators) is correlated with fear of other dangers (e.g., humans, pathogens, moving vehicles, or fire). We discuss why fear generalization should be ecologically important, and why we expect fear to correlate across disparate dangers. CIDs in fear are well studied for some dangers in some taxa (e.g., human fear of pathogens), but not well studied for most dangers. Fear of some dangers has been found to correlate with general fearfulness, but some cases where we might expect correlated fears (e.g., between fear of humans, familiar predators, and exotic predators) are surprisingly understudied.     

Lesser of Two Evils? Foraging Choices in Response to Threats of Predation and Parasitism

Predators have documented post-encounter (density-mediated) effects on prey but their pre-encounter impacts, including behavioural alterations, can be substantial as well. While it is increasingly evident that this “ecology of fear” is important to understand for natural enemy-victim relationships, fear responses of hosts to the threat of infection by a parasite are relatively unknown. We examined larval amphibian (Lithobates pipiens) foraging choices by experimentally manipulating the presence of cues relating to predator (larval odonate) or parasite (the trematode Ribeiroia ondatrae) threats. Tadpoles avoided foraging where predator or parasite cues were present; however, they did not treat these as equal hazards. When both threats were simultaneously present, tadpoles strongly preferred to forage under the threat of parasitism compared to predation, likely driven by their relative lethality in our study. Our results indicate that altered spatial use is an important anti-parasite behaviour, and demonstrate that parasite avoidance can affect foraging in a manner similar to predators, warranting greater study of the pre-encounter effects of this enemy type.     

Silence resulting from the cessation of movement signals danger

Most of what we know about the neural basis of fear has been unravelled by studies using associative fear learning [1]. However, many animal species are able to use social cues to recognize threats [2,3], a defence mechanism that may be less costly than learning from self-experience. Most studies in the field have focused on species-specific signals, such as alarm calls or pheromones, remaining unclear whether more generic cues can mediate this process. Here we report that rats perceive the cessation of movement-evoked sound as a signal of danger and its resumption as a signal of safety. To study transmission of fear between rats we assessed the behavior of an observer while witnessing a demonstrator cage-mate display fear responses. Having tested a multitude of cues, we found that observer rats respond to an auditory cue which signals the sudden immobility of the demonstrator rat - the cessation of the sound of motion. As freezing is a pervasive fear response in animals [4,5], silence may constitute a truly public cue used by a variety of animals in the ecosystem to detect impeding danger.     

Nest Sanitation as the Evolutionary Background for Egg Ejection Behaviour and the Role of Motivation for Object Removal

Higher interclutch colour variation can evolve under the pressure of brood parasitism to increase the detection of parasitic eggs. Nest sanitation could be a prerequisite for the evolution of anti-parasite defence in terms of egg ejection. In this respect, we used nest sanitation behaviour as a tool to identify: i) motivation and its underlying function and, ii) which features provoke ejection behaviour. Therefore, we experimentally tested whether size, colour or shape may influence ejection behaviour using artificial flat objects. We found a high interclutch variation in egg colouration and egg size in our tree sparrow (Passer montanus) population. Using colour and size we were in fact able to predict clutch affiliation for each egg. Our experiments further revealed the existence of direct anti-parasite behaviours and birds are able to recognise conspecific eggs, since only experimentally-deposited eggs have been removed. Moreover, experiments with different objects revealed that the motivation of tree sparrows to remove experimental objects from their nests was highest during egg laying for objects of varying size, most likely because of parasitism risk at this breeding stage. In contrary, motivation to remove white objects and objects with edges was higher during incubation stage as behavioural patterns connected to hatching started to emerge. The fact that rejection rate of our flat objects was higher than real egg ejection, suggests that egg ejection in tree sparrows and probably more general in small passerines, to be limited by elevated costs to eject eggs with their beaks. The presence of anti-parasite behaviour supports our suggestion that brood parasitism causes variation in egg features, as we have found that tree sparrows can recognise and reject conspecific eggs in their clutch. In conclusion, in tree sparrows it seems that nest sanitation plays a key role in the evolution of the removal of parasitic eggs.     

Emotional facial expression detection in the peripheral visual field

Background

In everyday life, signals of danger, such as aversive facial expressions, usually appear in the peripheral visual field. Although facial expression processing in central vision has been extensively studied, this processing in peripheral vision has been poorly studied.

Methodology/Principal Findings

Using behavioral measures, we explored the human ability to detect fear and disgust vs. neutral expressions and compared it to the ability to discriminate between genders at eccentricities up to 40°. Responses were faster for the detection of emotion compared to gender. Emotion was detected from fearful faces up to 40° of eccentricity.

Conclusions

Our results demonstrate the human ability to detect facial expressions presented in the far periphery up to 40° of eccentricity. The increasing advantage of emotion compared to gender processing with increasing eccentricity might reflect a major implication of the magnocellular visual pathway in facial expression processing. This advantage may suggest that emotion detection, relative to gender identification, is less impacted by visual acuity and within-face crowding in the periphery. These results are consistent with specific and automatic processing of danger-related information, which may drive attention to those messages and allow for a fast behavioral reaction.     

Attitudes toward Animals among German Children and Adolescents

ABSTRACT

This is the first study about attitudes toward animals among German children and adolescents. A sample of 543 pupils (261 boys, 282 girls) aged 11 to 17 (mean age = 13.37 ± 2.01 years) completed a questionnaire based on different established scales, for example, the Animal Attitude Scale (AAS) and the Intermediate Attitude Scale (IAS). Several aspects of attitudes toward animals and various dimensions of human–animal relationships were measured, including gender, age, grade, pet ownership, animal-related activities, meat consumption, and fear of and disgust toward animals. Gender and age were important factors in determining attitudes toward animals: pro-animal attitudes decreased with age and girls showed more positive attitudes compared with boys. Pet ownership and animal-related activities were associated with more positive attitudes toward animals, whilst meat consumption was related to lower pro-animal attitudes. There were no correlations between fear and general attitudes toward animals. The correlations between disgust and attitudes toward animals were weak. We found significant correlations among the different scales and subscales in animal attitudes.