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.     

The association between disgust, danger and fear of macroparasites and human behaviour

Evolutionary explanations of disgust propensity propose that disgust is an adaptation which helps us to decrease the likelihood of being infected by pathogens. To test this hypothesis, we examined human fear, disgust and self-perceived danger as a response on colourful pictures of disease-relevant and disease-irrelevant invertebrates. Furthermore, we also examined a possible link between these variables and human anti-parasite behaviour. We found that participants clearly distinguished between disease-relevant and disease-irrelevant group of animals, and that females always scored higher than males. Moreover, there were associations between ratings of fear, disgust and danger and human anti-parasite behaviour. Our results support the hypothesis that human emotions and behaviours are shaped by natural selection.     

Chemosignals of fear enhance cognitive performance in humans

It is well documented across phyla that animals experiencing stress and fear produce chemical warning signals that can lead to behavioral, endocrinological, and immunological changes in the recipient animals of the same species. Humans distinguish between fear and other emotional chemosignals based on olfactory cues. Here, we study the effect of human fear chemosignals on the speed and accuracy of cognitive performance. In a double-blind experiment, female participants performed a word-association task while smelling one of the three types of olfactory stimuli: fear sweat, neutral sweat, and control odor carrier. We found that the participants exposed to the fear condition performed more accurately and yet with no sacrifice for speed on meaningful word conditions than those under either the neutral or the control condition. At the same time, they performed slower on tasks that contained ambiguous content. Possible factors that could introduce bias, such as individual differences due to anxiety, verbal skills, and perceived qualities of the smells, were ruled out. Our results demonstrate that human fear chemosignals enhance cognitive performances in the recipient. We suggest that this effect originates from learned associations, including greater cautiousness and concomitant changes in cognitive strategies.     

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.     

Proactive strategies to avoid infectious disease

Infectious disease exerts a large selective pressure on all organisms. One response to this has been for animals to evolve energetically costly immune systems to counter infection, while another--the focus of this theme issue--has been the evolution of proactive strategies primarily to avoid infection. These strategies can be grouped into three types, all of which demonstrate varying levels of interaction with the immune system. The first concerns maternal strategies that function to promote the immunocompetence of their offspring. The second type of strategy influences mate selection, guiding the selection of a healthy mate and one who differs maximally from the self in their complement of antigen-coding genes. The third strategy involves two classes of behaviour. One relates to the capacity of the organisms to learn associations between cues indicative of pathogen threat and immune responses. The other relates to prevention and even treatment of infection through behaviours such as avoidance, grooming, quarantine, medicine and care of the sick. In humans, disease avoidance is based upon cognition and especially the emotion of disgust. Human disease avoidance is not without its costs. There is a propensity to reject healthy individuals who just appear sick--stigmatization--and the system may malfunction, resulting in various forms of psychopathology. Pathogen threat also appears to have been a highly significant and unrecognized force in shaping human culture so as to minimize infection threats. This cultural shaping process--moralization--can be co-opted to promote human health.     

How perceived threat increases synchronization in collectively moving animal groups

Nature is rich with many different examples of the cohesive motion of animals. Previous attempts to model collective motion have primarily focused on group behaviours of identical individuals. In contrast, we put our emphasis on modelling the contributions of different individual-level characteristics within such groups by using stochastic asynchronous updating of individual positions and orientations. Our model predicts that higher updating frequency, which we relate to perceived threat, leads to more synchronized group movement, with speed and nearest-neighbour distributions becoming more uniform. Experiments with three-spined sticklebacks (Gasterosteus aculeatus) that were exposed to different threat levels provide strong empirical support for our predictions. Our results suggest that the behaviour of fish (at different states of agitation) can be explained by a single parameter in our model: the updating frequency. We postulate a mechanism for collective behavioural changes in different environment-induced contexts, and explain our findings with reference to confusion and oddity effects.     

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.     

Smell, learn and live: The role of chemical alarm cues in predator learning during early life history in a marine fish

The speed with which individuals can learn to identify and react appropriately to predation threats when transitioning to new life history stages and habitats will influence their survival. This study investigated the role of chemical alarm cues in both anti-predator responses and predator identification during a transitional period in a newly settled coral reef damselfish, Pomacentrus amboinensis. Individuals were tested for changes in seven behavioural traits in response to conspecific and heterospecific skin extracts. Additionally, we tested whether fish could learn to associate a previously novel chemical cue (i.e. simulated predator scent) with danger, after previously being exposed to a paired cue combining the conspecific skin extract with the novel scent. Fish exposed to conspecific skin extracts were found to significantly decreased their feeding rate whilst those exposed to heterospecific and control cues showed no change. Individuals were also able to associate a previously novel scent with danger after only a single previous exposure to the paired conspecific skin extract/novel scent cue. Our results indicate that chemical alarm cues play a large role in both threat detection and learned predator recognition during the early post-settlement period in coral reef fishes.     

Frequency and recency of infection and their relationship with disgust and contamination sensitivity

Both disgust and contamination sensitivity likely evolved to protect us from infectious disease. Paradoxically, disgust may be reduced by frequent exposure to disgust-inducing cues — cues most likely to occur in disease-rich environments. In this study, we examined whether more frequent or recent illness might act to reverse this process. To test this, we surveyed 616 adults, obtaining illness frequency and recency data, disgust and contamination sensitivity, and a variety of control measures. Heightened contamination sensitivity was associated with more frequent infectious illness, but not with recency of infection. We also found that participants who had heightened contamination sensitivity and who were also more disgust sensitive had significantly fewer recent infections. These findings suggest that frequent illness may up-regulate contamination sensitivity potentially counteracting the effects of exposure on disgust. More importantly, these data provide the first direct evidence of a protective effect of contamination and disgust, against infectious disease.     

Disease avoidance as a functional basis for stigmatization

Stigmatization is characterized by chronic social and physical avoidance of a person(s) by other people. Infectious disease may produce an apparently similar form of isolation-disease avoidance-but on symptom remission this often abates. We propose that many forms of stigmatization reflect the activation of this disease-avoidance system, which is prone to respond to visible signs and labels that connote disease, irrespective of their accuracy. A model of this system is presented, which includes an emotional component, whereby visible disease cues directly activate disgust and contamination, motivating avoidance, and a cognitive component, whereby disease labels bring to mind disease cues, indirectly activating disgust and contamination. The unique predictions of this model are then examined, notably that people who are stigmatized evoke disgust and are contaminating. That animals too show avoidance of diseased conspecifics, and that disease-related stigma targets are avoided in most cultures, also supports this evolutionary account. The more general implications of this approach are then examined, notably how it can be used to good (e.g. improving hygiene) or bad (e.g. racial vilification) ends, by yoking particular labels with cues that connote disease and disgust. This broadening of the model allows for stigmatization of groups with little apparent connection to disease.     

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.     

Evidence that disgust evolved to protect from risk of disease

Disgust is a powerful human emotion that has been little studied until recently. Current theories do not coherently explain the purpose of disgust, nor why a wide range of stimuli can provoke a similar emotional response. Over 40 000 individuals completed a web-based survey using photo stimuli. Images of objects holding a potential disease threat were reported as significantly more disgusting than similar images with little or no disease relevance. This pattern of response was found across all regions of the world. Females reported higher disgust sensitivity than males; there was a constant decline in disgust sensitivity over the life course; and the bodily fluids of strangers were found more disgusting than those of close relatives. These data provide evidence that the human disgust emotion may be an evolved response to objects in the environment that represent threats of infectious disease.     

The Sound of Danger: Threat Sensitivity to Predator Vocalizations,Alarm Calls,and Novelty in Gulls

The threat sensitivity hypothesis predicts that organisms will evaluate the relative danger of and respond differentially to varying degrees of predation threat. Doing so allows potential prey to balance the costs and benefits of anti-predator behaviors. Threat sensitivity has undergone limited testing in the auditory modality, and the relative threat level of auditory cues from different sources is difficult to infer across populations when variables such as background risk and experience are not properly controlled. We experimentally exposed a single population of two sympatric gull species to auditory stimuli representing a range of potential threats in order to compare the relative threat of heterospecific alarm calls, conspecific alarms calls, predator vocalizations, and novel auditory cues. Gulls were able to discriminate among a diverse set of threat indicators and respond in a graded manner commensurate with the level of threat. Vocalizations of two potential predators, the human voice and bald eagle call, differed in their threat level compared to each other and to alarm calls. Conspecific alarm calls were more threatening than heterospecfic alarm calls to the larger great black-backed gull, but the smaller herring gull weighed both equally. A novel cue elicited a response intermediate between known threats and a known non-threat in herring gulls, but not great black-backed gulls. Our results show that the relative threat level of auditory cues from different sources is highly species-dependent, and that caution should be exercised when comparing graded and threshold threat sensitive responses.     

A tradeoff between perceived predation risk and energy conservation revealed by an immune challenge experiment

Energy is typically a limiting factor for animals during boreal winters, when low temperatures increase the cost of thermoregulation at the same times as short day‐lengths and snow cover constrain foraging opportunities. Under these circumstances animals use a suite of behavioural and physiological adaptations to avoid overnight starvation. However, it is poorly understood how such strategies are affected by increased energy demands from other physiological systems. Thus, we used free‐ranging blue tits, Cyanistes caeruleus, to test if competing demands for energy (here induced by a non‐inflammatory, antibody‐mediated immune challenge) would affect nocturnal body temperature (a predictor of energy expenditure in small animals) and energy‐saving nest box roosting behaviour. We also assessed if the immune challenge incurred long‐term survival costs. We found no evidence that body temperature regulation differed between immune‐challenged and saline‐injected birds. Nor did the immune challenge reduce survival to the next breeding season. However, old (second winter or older) immune‐challenged birds continued roosting in nest boxes to a larger extent at the peak immune response, despite increased perceived predation risk induced by the preceding capture and immunization. In contrast, old control birds were less prone to roost in nest boxes after capture and saline injection. This difference was less pronounced in young (first winter) birds. We interpret the increased risk‐taking behaviour in immune‐challenged birds as a consequence of a higher need for exploiting the thermal benefits of nest box roosting to reduce energy loss. This suggests that resource deficiency might be a stronger predictor of overnight survival than the threat of nocturnal predation in this system. As such, our study provides insights into the classic tradeoff between starvation and predation risk, in suggesting that priority is given to minimizing the risk of starvation in situations where both starvation and predation risks increase during cold winter nights.     

Why disgust matters

The new synthesis about disgust is that it is a system that evolved to motivate infectious disease avoidance. There are vital practical and intellectual reasons why we need to understand disgust better. Practically, disgust can be harnessed to combat the behavioural causes of infectious and chronic disease such as diarrhoeal disease, pandemic flu and smoking. Disgust is also a source of much human suffering; it plays an underappreciated role in anxieties and phobias such as obsessive compulsive disorder, social phobia and post-traumatic stress syndromes; it is a hidden cost of many occupations such as caring for the sick and dealing with wastes, and self-directed disgust afflicts the lives of many, such as the obese and fistula patients. Disgust is used and abused in society, being both a force for social cohesion and a cause of prejudice and stigmatization of out-groups. This paper argues that a better understanding of disgust, using the new synthesis, offers practical lessons that can enhance human flourishing. Disgust also provides a model system for the study of emotion, one of the most important issues facing the brain and behavioural sciences today.     

Fear influences perceived reaching to targets in audition,but not vision

The superordinate mechanism view of emotions predicts that fear should influence perception to carry out the evolved function of overcoming immediate threats. Previous work demonstrates that fear does adaptively influence visual perception. However, there are recurring situations in which auditory perception is used for overcoming immediate threats (e.g., avoiding predators after dark). Some research suggests that the auditory system, independent of fear, is adaptively biased to hear approaching sounds as closer than equidistant receding sounds (a.k.a. the looming bias). The present study investigated whether fear, as a superordinate mechanism, influences auditory perception such that sounds are perceived to be closer, ultimately providing an advantage when avoiding immediate threats. Participants judged whether or not they could reach to an aurally or visually perceived target while either in a fearful or neutral state. The results demonstrated that while in a fearful state, participants judged targets to be closer to them, but only when the target was perceived aurally. This finding extends previous work on adaptive biases in auditory perception to include the influence of fear.     

Behavioral Immune System and Ingroup Derogation: The Effects of Infectious Diseases on Ingroup Derogation Attitudes

From evolutionary reasoning, we derived a novel hypothesis that ingroup derogation is an evolved response of behavioral immune system which follows the smoke detector principle and the functional flexibility principle. This hypothesis was tested and supported across three experiments. In Experiment 1, participants’ group membership was manipulated by using a minimal group paradigm. The results indicated that mere social categorization alone — a heuristic cue that implies the differentiation between "us" and "them" — was sufficient to elicit ingroup derogation among Chinese participants, and, such an intergroup bias was positively associated with the perceived vulnerability to diseases, which was also more consistently associated with ingroup attitudes. Experiment 2 extended and partially replicated Experiment 1 by showing that when there were cues of diseases in the immediate physical environment, Chinese participants exaggerated their attitudes of ingroup derogation. The results also showed that this effect was mainly driven by outgroup attraction. Experiment 3 changed the method of disease manipulation, and found that Chinese participants responded more strongly to disease cues originating from ingroup members and that they endorsed more ingroup derogation attitudes even when the ingroup and outgroup members were both displaying cues of diseases. Taken together, these results reveal the previously unexplored effects of infectious diseases on ingroup derogation attitudes, and suggest an interesting linkage between the evolved behavioral immune system and the ingroup derogation.     

Effects of Having Pets at Home on Children's Attitudes toward Popular and Unpopular Animals

ABSTRACT

Having pets at home provides various social, health, and educational benefits to children. The question of how keeping pets at home affects the attitudes of children toward wild animals still has not been answered, due to various methodological issues, such as ignorance of some attitude dimensions and/or questionnaires that include items focused on very different animals. We conducted three independent research surveys (using three independent samples) of Slovakian primary school children aged 10 to 15 years (n = 1297). These surveys focused on the effects of keeping pets on the attitudes of children towards, and knowledge of, three unpopular animals in Slovakia. These animals were pests (potato beetle) (Study 1), predators (wolf) (Study 2), and those that pose a threat of disease to humans (mouse) (Study 3). Each survey also included a popular animal (ladybird beetle, rabbit, and squirrel, respectively), which served as a “control”; these were compared by pair-wise statistics. Results consistently showed that children had better knowledge of, but less favorable attitudes towards, unpopular animals compared with popular ones. Having pets at home was associated with more positive attitudes to, and better knowledge of, both popular and unpopular animals. Girls were less favorably inclined than boys to animals that may pose a threat, danger, or disease to them. Implications for humane education are discussed, especially in terms of keeping pets, the link between knowledge and attitudes, and children's understanding of ecological adaptations.     

Sleeping birds do not respond to predator odour

Background

During sleep animals are relatively unresponsive and unaware of their environment, and therefore, more exposed to predation risk than alert and awake animals. This vulnerability might influence when, where and how animals sleep depending on the risk of predation perceived before going to sleep. Less clear is whether animals remain sensitive to predation cues when already asleep.

Methodology/Principal Findings

We experimentally tested whether great tits are able to detect the chemical cues of a common nocturnal predator while sleeping. We predicted that birds exposed to the scent of a mammalian predator (mustelid) twice during the night would not go into torpor (which reduces their vigilance) and hence would not reduce their body temperature as much as control birds, exposed to the scent of another mammal that does not represent a danger for the birds (rabbit). As a consequence of the higher body temperature birds exposed to the scent of a predator are predicted to have a higher resting metabolic rate (RMR) and to lose more body mass. In the experiment, all birds decreased their body temperature during the night, but we did not find any influence of the treatment on body temperature, RMR, or body mass.

Conclusions/Significance

Our results suggest that birds are not able to detect predator chemical cues while sleeping. As a consequence, antipredatory strategies taken before sleep, such as roosting sites inspection, may be crucial to cope with the vulnerability to predation risk while sleeping.     

The behavioural immune system and the psychology of human sociality

Because immunological defence against pathogens is costly and merely reactive, human anti-pathogen defence is also characterized by proactive behavioural mechanisms that inhibit contact with pathogens in the first place. This behavioural immune system comprises psychological processes that infer infection risk from perceptual cues, and that respond to these perceptual cues through the activation of aversive emotions, cognitions and behavioural impulses. These processes are engaged flexibly, producing context-contingent variation in the nature and magnitude of aversive responses. These processes have important implications for human social cognition and social behaviour-including implications for social gregariousness, person perception, intergroup prejudice, mate preferences, sexual behaviour and conformity. Empirical evidence bearing on these many implications is reviewed and discussed. This review also identifies important directions for future research on the human behavioural immune system--including the need for enquiry into underlying mechanisms, additional behavioural consequences and implications for human health and well-being.