Original ArticleSpiders at the cocktail party: an ancestral threat that surmounts inattentional blindness
Introduction
In our daily, modern life, the ability to maintain focused attention to tasks despite numerous potential distractions is a highly desirable ability. However, critical events may require an interruption of our focused attention despite their irrelevance to any exigent goals and expectations (Most, Scholl, Clifford, & Simons, 2005). Such critical events can be physical and non-conceptual. For instance, looming objects provoke automatic responses for avoiding bodily injury such as reflexive orienting (Franconeri & Simons, 2003), defensive eye blinks (Yonas, 1981), and avoidant head jerks (Yonas et al., 1977). Another large class of important events is of a learned, conceptual, and personal nature. In the famous “cocktail party” effect, for example, our name said aloud in a neighboring conversation strongly commands our attention (Wood & Cowan, 1995). We propose that the visual system may be inherently prepared to orient attention to a third class of events — specific types of objects that have been of recurring and immediate importance over evolutionary time (Coss and Goldthwaite, 1995, New et al., 2007, Tooby and Cosmides, 1990).
Emotional disorder researchers have long-debated whether the high frequency of fears and phobias for ecological threats such as snakes and spiders reflect a “biological preparedness” for detecting and surviving the persistently recurring hazards of our ancestral environments (Marks and Nesse, 1994, Öhman and Mineka, 2001, Seligman, 1971). Some of the most directly studied examples of this kind are angry faces (e.g. Öhman, Lundqvist, & Esteves, 2001), snakes (e.g. Öhman & Mineka, 2003), and spiders (Öhman, Flykt, & Esteves, 2001), each of which has been advanced as model instances of biologically prepared fears.
Human faces, though, are at least as important in modern society as they have been in ancestral environments, which complicates the attribution of their attentional capture to ontogenetic or phylogenetic causes. Spiders, on the other hand, rarely constitute a serious physical threat to people today. Only about 200 of the approximately 40,000 extant spider species pose serious medical concerns to healthy adults by envenomating bites (Diaz, 2004). Medically confirmed fatalities are extremely rare — around six annually in the U.S. (Langley, 2005) and less than 200 annually worldwide (Russell, 1991).
Yet, the spider genus, Latrodectus (the widow spiders), presents a particularly illustrative case for the commonly held – but rarely examined – assumption that spiders were a persistent and potentially injurious feature of humans’ ancestral environments. Species of Latrodectus are now found on every continent (except Antarctica), however, there is a particularly high density of species in southern Africa were they likely originated (Garb, González, & Gillespie, 2004). Although there is little or no fossil evidence of Latrodectus, amber fossil specimens of its closest sister genus, Steatoda (Arnedo, Coddington, Agnarsson, & Gillespie, 2004), have been dated to the mid-Eocene epoch (48.6–40.4 million years ago; Berland, 1939, Petrunkevitch, 1942). For comparison, an ancient predatory threat to primates, snakes, evolved envenomating bites by 60 million years ago (Vidal, 2002). Their continuous coexistence with the catarrhine species (Old World monkeys and apes) may have compelled profound evolutionary changes to those primate species’ perceptual systems in order to detect snakes pre-attentively — rather than evolve a venom resistance like other mammals (Isbell, 2006, Le et al., 2013). Unfortunately, comparative and paleobiological evidence is not likely to uncover when – or the first ancestral species in which – a behaviorally identifiable snake or spider “detector” might have first arose (but see Isbell, 2006 for review).
Although there are still far more snake bites and fatalities (Kasturiratne et al., 2008), the effects of widow spider bite envenomation, termed latrodectism, are considered to be the most medically important spider bite syndrome worldwide (Graudins et al., 2012). Widow spider venom contains a phylogenetically unique and extremely potent neurotoxin, α-latrotoxin, whose effects are specific to vertebrates — even though widow spiders primarily prey on invertebrates (Garb & Hayashi, 2013). α-Latrotoxin originated in a common ancestor of the Latrodectus and Staetoda genus (e.g. false black widows) but evolved a far greater vertebrate-specific toxicity in Latrodectus soon after their divergence (Garb & Hayashi, 2013). In humans, α-latrotoxin produces severe muscle pain, cramps, nausea and other complications that can be incapacitating for days and remain debilitating for weeks thereafter (Maretić, 1983). Since the advent of antivenom, mortality rates are less than 1%, but reports for pre-antivenom populations range from 4% to 8% for healthy adults (Bettini, 1964). Widow spider bites pose an even more significant physical threat to pregnant (Russell et al., 1979, Wolfe et al., 2011), young, elderly, and infirm individuals (Müller, 1992).
In the consideration of just one spider genus, it appears that a number of Latrodectus species with potent, vertebrate-specific venoms populated Africa long before hominoids and cercopithecoids diverged (Steiper, Young, & Sukarna, 2004) and have coexisted there with hominoids for tens of millions of years since. This increasing paleobiological evidence corroborates the common presumption that humans were at perennial, unpredictable, and significant risk of encountering highly venomous spiders in their ancestral environments. Even when not fatal, a widow spider bite in the ancestral world would often still leave one incapacitated for days or even weeks — terribly exposed to other dangers and/or a considerable burden to family and friends.
But avoiding spiders and such serious consequences is not difficult, providing they are noticed in time. Widow spiders, though, are typically darkly-colored (black or brown) with body lengths as small as 8 mm and typically hide in dark recesses. Detection, therefore, is the critical arbiter of success in such encounters — any improvements to the sensitivity, vigilance, reliability, and speed of faculties for their detection would have been of significant selective advantage. Proponents of the Snake Detector theory have similarly reasoned that predation from snakes primarily drove catarrhine species towards more sophisticated detection abilities rather than physical defenses such as a physiological resistance to venoms (Isbell, 2006, Le et al., 2013). The perceptual mechanisms for avoiding venomous bites appear to be more cost-effective than the physiological measures necessary to survive them asymptomatically.
Since spiders were of far greater significance to survival in ancestral environments than they are in today’s environment, they constitute a uniquely well-suited test category of inherent – that is, not acquired – attentional priorities (New et al., 2007). Any ability of these ancestral threats to capture attention and awareness may persevere today – despite their infrequency and inconsequentiality to modern life – as adapted behavioral vestiges of our visual cognitive systems: not as attentional priorities acquired haphazardly through experience (Coss & Goldthwaite, 1995).
Spiders and snakes have been examined with most of the paradigms used to measure attentional capture – though often with mixed results. In the most-used paradigm, visual search, spiders and snakes have been inferred to capture visual attention via their efficient detection in visual search tasks (LoBue and DeLoache, 2008, Öhman, Flykt and Esteves, 2001, Pflugshaupt et al., 2005). However, other visual search studies have suggested that such ready detection might be common to all animals, both threatening and nonthreatening (Jackson and Calvillo, 2013, Lipp et al., 2004, Tipples et al., 2002), or to all threatening objects, both ancestral and modern (Blanchette, 2006, Brosch and Sharma, 2005).
There are many factors involved in the visual search task that can complicate the inference of attentional capture. Visual searches are conducted with top-down guidance (Wolfe, Horowitz, Kenner, Hyle, & Vasan, 2004) and search templates (Schmidt & Zelinsky, 2009) that can differ in effectiveness between categories of real-world objects (Levin, Takarae, Miner, & Keil, 2001). Further, training can imbue entirely neutral targets with attention-recruiting properties (Kyllingsbæk et al., 2001, Shiffrin and Schneider, 1977), and the visual search task itself commonly broadens the distribution of attention which can generally increase detection efficiency (Belopolsky, Zwaan, Theeuwes, & Kramer, 2007). Therefore, the efficient detection of any such categories of objects (e.g. snakes, butterflies, and needles) in conventional visual search tasks may not clearly adjudicate between objects that automatically capture attention and awareness, and those whose detection is mediated by a combination of implicit and explicit factors (Cave and Batty, 2006, Most et al., 2005).
In a related paradigm, the irrelevant singleton task, the addition of spiders to an array interfered with viewers’ searches for a target object — despite the spiders’ irrelevance to the prescribed task. However, butterflies did so as well, and the apparent diversion of attention from the prescribed task to both animals was especially pronounced in individuals highly fearful of spiders (Devue, Belopolsky, & Theeuwes, 2011). The expectation that spiders would be displayed increased the spider-fearful participants’ monitoring for – and interference by – both fear-relevant and neutral stimuli. Yet, even those especially fearful individuals were capable of ignoring the appearance of additional objects when spiders were very unlikely to appear. Such probability information – deducible from repeated presentations of salient stimuli – can guide attention and monitoring whenever (Devue et al., 2011) and wherever warranted (Notebaert, Crombez, Van Damme, De Houwer, & Theeuwes, 2010).
The evidence for ancestral threats being prepared – or inherently prioritized – for attention is thus generally mixed but also commonly complicated by top-down information and guidance. Undoubtedly, the ability to quickly find threats of all kinds when trying or alerted to do so is of great survival value. However, dangers such as spiders and snakes occur unpredictably and generally so infrequently that they need to be detected and brought to awareness largely absent any foreknowledge, intentions, or expectations. To minimize such top-down control, the current study presented spiders – a prototypical ancestral threat – using the inattentional blindness (IB) paradigm. Here, an unexpected stimulus is presented peripherally to – and coincidentally with – a central, task-related stimulus (Newby & Rock, 1998). The experimental stimulus is only tested in one trial for each participant, since even one presentation of a stimulus can facilitate the detection of subsequent occurrences via priming (Tulving & Schacter, 1990) and/or expectations (Mack & Rock, 1998). The IB paradigm is thus a very rigorous measure of attentional capture relative to approaches that repeatedly display experimental stimuli. Importantly, the IB task more closely emulates the conditions under which humans have typically encountered spiders and snakes in their ancestral and modern environments, that is, largely without foreknowledge, warning, or task-relevance.
The IB paradigm can not only measure how likely unexpected objects are to be detected, but which of their qualities (e.g. location, shape) are registered during their single, brief exposure. The real-world function of attentional capture is to recognize significant objects and events and prompt some adaptive response. The ability to divert attention from current tasks is a necessary but not sufficient quality of threatening objects and events, whether ancestral or modern. As Most and colleagues reason, should a child appear in front of your car as you tune the radio, the important result is not that you are slower turning the radio knob, it is that you steer away from the child (2005). The threshold of success for perceiving threats is particularly high: that is to become aware of their presence, their location, and critically for reacting adaptively — their identity. Being distracted from a possibly crucial task while remaining unaware of the potential threat constitutes the worst of both worlds.
In light of their evolutionarily-persistent threat to survival, spiders are hypothesized to be exceptionally capable of capturing attention and propagation into conscious awareness even when completely unexpected and irrelevant to any exigent goals. We predicted that iconic, prototypical spiders (Fig. 1A and C) will be very frequently detected, located, and identified when presented in an inattentional blindness task. This was tested in a first experiment and close conceptual replication along with items of visual and categorical interest for comparison.
A number of stimuli were included in both experiments to control for the iconic spiders’ lower-level visual characteristics and to closely delimit some visual features that may be integral to their efficient detection. Seminal research on IB suggested that the shapes of most simple objects presented under these display conditions go largely unregistered (Mack & Rock, 1998). However, the exact shape of some highly meaningful objects significance such as the participants’ own names can be closely specified through overlearning and are readily detected (Mack et al., 2002, Mack and Rock, 1998). Whereas our own written name is specified through experience, for example, some objects of persisting biological importance and visual typicality – such as faces and spiders – may be inherently specified in a template-like fashion (Öhman & Mineka, 2001). These perceptual templates may be triggered pre-attentively by detecting some specific configuration of simple visual features (Öhman, 2008). In one study that largely precluded conditioning experiences, 5-month olds were found to attend stimuli falling within a perceptual template of spiders more than to different configurations of the same visual elements (Rakison & Derringer, 2008).
The defining visual configuration of spiders appears to be the radiation of multiple segments from a central mass point with “legginess” being the most frequently reported frightening feature by spider-fearful individuals (Aronoff et al., 1988, Davey, 1992). This suggests that a “spider template” should encompass the range of configurations in which spiders naturally appear, including “curled up”, even when such a stimulus is explicitly categorized as an innocuous flower — a manipulation following Vuilleumier and Schwartz (2001). We predicted that the display of a clover-like object in Experiment 1 (Fig. 1B) – formed through reorganization of the prototypical spider’s features (Fig. 1A) – would satisfy the purported spider template and capture attention and awareness in the same fashion as the prototypical spider. In Experiment 2, the prototypical spider (Fig. 1C) was reorganized so that many segments were chained together rather than radiate directly from the central mass — differing critically from the spider template (Fig. 1D). This configuration was predicted to be unlikely to capture attention and awareness despite its preservation of all of the prototypical spider’s lower- and mid-level visual attributes that are important for object recognition (e.g. vertices, line junctions and terminations; Biederman, 1987, Gibson et al., 2007, Szwed et al., 2009).
The spider template may not require curvilinear features, even though curvilinearity is more characteristic of living things than nonliving things (Kurbat, 1997) and which can guide their detection in visual search tasks (Levin et al., 2001). To test whether curvilinearity is integral to the spider template, rectilinear versions of each prototypical spider were constructed for both experiments. These rectilinear variants were composed entirely of straight lines and rectangles comparable to the sizes and lengths of the original curvilinear features (Experiment 1: Fig. 1E; Experiment 2: Fig. 1G). These rectilinear spiders were predicted to fall within the spider template and consequently often capture attention and awareness.
To control for visual salience, three additional items were constructed by reconfiguration of both rectilinear spiders’ radiating segments (Fig. 1F in Experiment 1; Fig. 1H in Experiment 2) and by enclosure of the Experiment 1’s rectilinear spider with additional segments (Fig. 1I). Although resulting, in the latter case, in increased salience in terms of area and number of features these stimuli were all predicted to fall outside of the spider template and thus be more susceptible to inattentional blindness.
To evaluate another evolutionarily-motivated account of attentional biases, the animate-monitoring hypothesis (New et al., 2007, New et al., 2010), a second animal (housefly: Fig. 1J) was included in Experiment 2 along with its scrambled visual control (Fig. 1K). In this account, people and animals have been of such longstanding importance to survival that they have become an inherent priority for visual attention and monitoring categorically. Participants shown two rapidly alternating scenes more quickly and frequently detected changes to animate objects – including people and animals of all kinds – than changes made to inanimate objects such as tools, plants, or buildings. Without any direction as to the category of the target objects – unlike that provided in visual search – participants’ spontaneous selections for attention were strongly and immediately biased to animate objects. Some visual search studies have also found fear-irrelevant animals (e.g. horses) to be found more efficiently than inanimate objects (Jackson and Calvillo, 2013, Lipp et al., 2004, Tipples et al., 2002).
The animate-monitoring hypothesis espouses that animate objects are inherently prioritized for visual attention. However, only a few forms such as the human face and figure, snakes, and spiders have likely been of sufficient structural invariance, temporal persistence, and potential threat to bring about a corresponding perceptual template for their detection (Blumstein et al., 2000, Coss and Goldthwaite, 1995, Öhman and Mineka, 2001). The appearance of other animals would – given the diversity and mutability of their forms – likely have to be learned through personal experience or social learning (Barrett & Broesch, 2012). It is predicted here that spiders – by virtue of a dedicated perceptual template – will be uniquely capable of capturing attention and awareness under conditions in which other animals (i.e. housefly) will often go undetected.
Finally, the rapid detection and awareness of spiders could conceivably be a result of more general pathways for learning about threatening objects such as conditioning and modeling (Rachman, 1977). If such attentional biases are largely developed through personal experience, hypodermic needles should often be feared and capable of capturing attention and awareness, since injected vaccinations are the rule, and spider bites the rare exception in modern society. When surveyed explicitly, hypodermic needles are generally comparable to spiders in terms of rated fearfulness (Bernstein and Allen, 1969, Fredrikson et al., 1996).
If such attentional biases are mediated through aversive experiences, individuals’ reported fears of each type of threatening object (hypodermic needles or spiders) should predict how likely they are to detect, locate, and identify the object of their fear. Especially fearful individuals have demonstrated greater efficiency in visual searches for the objects they fear in some studies (Öhman, Flykt, & Esteves, 2001) but not others (Waters, Lipp, & Randhawa, 2011). An iconic hypodermic needle (Fig. 1L, N) and corresponding scrambled visual control (Fig. 1M, O) were included in Experiments 1 and 2 to test whether the capture of attention and awareness can be inculcated for modern threats via general learning pathways.
Section snippets
Participants
In Experiment 1, 252 undergraduate students (mean age = 19; range 18–22; 50% male, 50% female) participated in the experiment for credit in an introductory psychology course. Being included later than the original six items, the enclosed rectilinear spider was presented to an additional 36 participants in the inattention trial.
In Experiment 2, 320 undergraduate students (mean age = 19.5, range 17–37; 86% female, 14% male) participated in the experiment for credit in an introductory psychology
Results
Binary logistic regressions were computed for each of the dichotomous outcomes – target stimuli detection, location, and identification – with the target stimuli displayed in the critical “inattention” trial as the categorical predictor of performance. An additional dichotomous outcome, termed “full report”, was calculated as success in all three measures (detection, location, and identification) or failure in any measure and similarly regressed on the critical stimulus type. In Experiment 1,
Discussion
First and foremost, this study demonstrated that spiders – a model instance of an evolutionarily-persistent threat – are uniquely capable of capturing observers’ visual attention and awareness. Without any forewarning and despite their marginalized presentation, the prototypical spiders were detected, located, and identified by a majority of participants in both the original experiment and replication. Considerable evidence accrued with other approaches, notably the visual search and irrelevant
Supplementary Material
The following are the Supplementary data to this article.
References (84)
- et al.
From a comb to a tree: Phylogenetic relationships of the comb-footed spiders (Araneae, Theridiidae) inferred from nuclear and mitochondrial genes
Molecular Phylogenetics and Evolution
(2004) - et al.
Prepared social learning about dangerous animals in children
Evolution and Human Behavior
(2012) - et al.
Fear survey schedule (II): Normative data and factor analyses based upon a large college sample
Behaviour Research and Therapy
(1969) Epidemiology of latrodectism
Toxicon
(1964)- et al.
Threat-detection in child development: An evolutionary perspective
Neuroscience and Biobehavioral Reviews
(2011) - et al.
Spatial uniformities in visual search
Brain and Cognition
(1996) - et al.
Gender and age differences in the prevalence of specific fears and phobias
Behaviour Research and Therapy
(1996) - et al.
The black widow spider genus Latrodectus (Araneae: Theridiidae): Phylogeny, biogeography, and invasion history
Molecular Phylogenetics and Evolution
(2004) - et al.
Nonaccidental properties underlie shape recognition in mammalian and nonmammalian vision
Current Biology
(2007) - et al.
Cloning and activity of a novel alpha-latrotoxin from red-back spider venom
Biochemical Pharmacology
(2012)
Snakes as agents of evolutionary change in primate brains
Journal of Human Evolution
Can the recognition of living things really be selectively impaired
Neuropsychologia
Animal-related fatalities in the United States — An update
Wilderness and Environmental Medicine
And along came a spider: An attentional bias for the detection of spiders in young children and adults
Journal of Experimental Child Psychology
What we see: Inattention and the capture of attention by meaning
Consciousness and Cognition
Latrodectism: Variations in clinical manifestations provoked by Latrodectus species of spiders
Toxicon
Fear and fitness: An evolutionary analysis of anxiety disorders
Ethology and Sociobiology
Phobias and preparedness: The selective, automatic, and encapsulated nature of fear
Biological Psychiatry
The scope of social attention deficits in autism: Prioritized orienting to people and animals in static natural scenes
Neuropsychologia
Looking out for danger: An attentional bias towards spatially predictable threatening stimuli
Behaviour Research and Therapy
Hypervigilance-avoidance pattern in spider phobia
Anxiety Disorders
Contributions of the amygdala to emotion processing: From animal models to human behavior
Neuron
Non-associative fear acquisition: A review of the evidence from retrospective and longitudinal research
Behaviour Research and Therapy
The conditioning theory of fear-acquisition: A critical examination
Behaviour Research and Therapy
Do infants possess an evolved spider-detection mechanism?
Cognition
Black widow spider envenomation during pregnancy. Report of a case
Toxicon
Exposure to disgust-evoking imagery and information processing biases in blood-injection-injury phobia
Behaviour Research and Therapy
Phobias and preparedness
Behavior Therapy
The role of invariant line junctions in object and visual word recognition
Vision Research
Disgust and disgust sensitivity in blood-injection-injury and spider phobia
Behaviour Research and Therapy
The past explains the present: Emotional adaptations and the structure of ancestral environments
Ethology and Sociobiology
How brains beware: Neural mechanisms of emotional attention
Trends in Cognitive Sciences
How fast can you change your mind? The speed of top-down guidance in visual search
Vision Research
A fear survey schedule for use in behaviour therapy
Behaviour Research Therapy
The recognition of threatening facial stimuli
Journal of Personality and Social Psychology
The size of an attentional window modulates attentional capture by color singletons
Psychonomic Bulletin & Review
Description de quelques arignées fossils
Revue Française d’Entomologie
Recognition-by-components: A theory of human image understanding
Psychological Review
Snakes, spiders, guns, and syringes: How specific are evolutionary constraints on the detection of threatening stimuli?
The Quarterly Journal of Experimental Psychology
Insular tammar wallabies (Macropus eugenii) respond to visual but not acoustic cues from predators
Behavioral Ecology
The role of fear-relevant stimuli in visual search: A comparison of phylogenetic and ontogenetic stimuli
Emotion
From searching for features to searching for threat: Drawing the boundary between preattentive and attentive vision
Visual Cognition
Cited by (71)
Inattentional blindness in dogs
2023, Applied Animal Behaviour ScienceNegative emotion-conditioned prepulse induces the attentional enhancement of prepulse inhibition in humans
2023, Behavioural Brain ResearchCitation Excerpt :Based on the view of prioritized processing for threaten-related negative emotions [63]. Negative emotions with threaten-related signals (motivationally relevant stimuli) play a crucial role in attracting attention under sensory competition conditions [18,21,46,50], which reflected by the larger amplitudes on the late positive components of ERPs compared with neutral or relaxing signals [31,54]. Many studies have found that negative emotions with threat-related stimuli and stimuli with conditioned negative emotions are more likely to attract attention, give priority to perceptual processing under sensory competition conditions, and activate more brain regions associated with processing emotions, e.g. middle superior temporal sulcus, amygdala, orbitofrontal cortex and cuneus [18,21,46,48,50].
Clarifying the effect of facial emotional expression on inattentional blindness
2022, Consciousness and CognitionCitation Excerpt :Whereas semantic value based on personal meaning seems to be very complex and flexible, one might assume a more stable semantic value when it is based on the evolutionary meaning of a stimulus. Previous studies have shown that semantic value based on the predetermined evolutionary meaning of threat (New & German, 2015) and semantic value based on personal overlearned meaning for onés name (Mack & Rock, 1998) indeed affect the susceptibility to inattentional blindness. Furthermore, the evolutionary predetermined semantic value based on facial emotional expression has been investigated in several studies and seems to increase noticing rates of unexpected objects.
Super-natural fears
2021, Neuroscience and Biobehavioral ReviewsCitation Excerpt :In some ways, these fears seem to have a similar developmental trajectory to other common fears such as blood, fire, strangers, separation, heights, social scrutiny, storms, thunder/lightning, or darkness, which are also especially common in childhood, and which we generally learn to overcome by adulthood (Coelho and Purkis, 2009; McNally, 1987; Zsido et al., 2019). They are considered to be biologically prepared or “hardwired” by evolution, in such a way that they only require a small extent of direct or indirect (vicarious/information-based) experience to be learned, cf. the theory of prepared learning (New and German, 2015; Seligman, 1971; Zsido et al., 2018a, b). Neuroscience suggests that common fears and phobias trigger threat detection survival circuits.
Clarifying the effect of facial emotional expression on inattentional blindness
2021, Consciousness and CognitionNo evidence of attentional prioritization for threatening targets in visual search
2024, Scientific Reports