Original Article
Spiders at the cocktail party: an ancestral threat that surmounts inattentional blindness

https://doi.org/10.1016/j.evolhumbehav.2014.08.004Get rights and content

Abstract

The human visual system may retain ancestral mechanisms uniquely dedicated to the rapid detection of immediate and specific threats (e.g. spiders and snakes) that persistently recurred throughout evolutionary time. We hypothesized that one such ancestral hazard, spiders, should be inherently prioritized for visual attention and awareness irrespective of their visual or personal salience. This hypothesis was tested using the inattentional blindness paradigm in which an unexpected and peripheral stimulus is presented coincidentally with a central task-relevant display. Despite their highly marginalized presentation, iconic spiders were nonetheless detected, localized, and identified by a very large proportion of observers. Observers were considerably less likely to perceive 1) different configurations of the same visual features which diverged from a spider prototype, or “template”, 2) a modern threatening stimulus (hypodermic needle) comparable in emotional salience, or 3) a different fear-irrelevant animal (housefly). Spiders may be one of a very few evolutionarily-persistent threats that are inherently specified for visual detection and uniquely “prepared” to capture attention and awareness irrespective of any foreknowledge, personal importance, or task-relevance.

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.

Raw Data - Experiment 1 and 2.

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