relative to the direction of movement (arrow). (Ewert 1968; cit 1984.).
Figure 2.4 The prey (a, c) vs. threat (b, d) configuration of a stripe traversing a common toad’s visual field in different directions (arrows). (Ewert et al. 1979; cit. Ewert 1984; cf. Suggested Reading, Movie A2.).
Tinbergen referred to such a stimulus, composed of different features, as a sign-stimulus. More generally, he pointed out that a feature A combined with a feature B may provide a certain sign-stimulus, but that feature A in combination with a feature C may provide a different sign-stimulus. For example, in male sticklebacks:
red belly and head-down posture addresses a threat signal to conspecific males, but not to females;
red belly and zigzag dance (Chapter 3) addresses a courtship signal to conspecific females, but not to males.
It is the combination—configuration or “Gestalt” (e.g., see Koffka 1922)—of behaviorally relevant features that determines the releasing value of a sign-stimulus in the sense of a “stimulus-pattern.” Its perception requires pattern recognition—a process, in which genetic and/or learning factors can be involved.
A configuration is perceived as the whole. This means that the sum of the responses to the features, when each feature is presented alone, is significantly less than the response to the complete array. Furthermore, recognition is independent of certain changes in other stimulus parameters as long as these do not affect the configuration. This phenomenon is called invariance.
Sign-stimuli provide parsimonious ways of encoding information to release adequately motivated behaviors. They also have survival value, since they are recognized quickly and responded to rapidly and unambigiously. With these attributes in mind, we continue to use the term sign-stimulus. Its efficacy can be analyzed in experiments using dummies by changing, omitting, adding, or exaggerating certain features.
Sign-stimuli allow humans to communicate with other animals. The wildlife biologist Kent Clegg used his ultralight aircraft as a sign-stimulus for captive-bred endangered whooping cranes, Grus americanus. Simulating their parents, he painted the wings of the plane white with black tips and thus instructed the young cranes to fly and follow the small aircraft. After leaving Idaho and making three overnight stops, he succeeded in having the young follow the plane on their first migratory trip at 35 mph—matching crane’s flight-speed—for 800 miles to their winter residence in New Mexico (see also https://friendsofthewildwhoopers.org/whooping-cranes-facts-management [accessed: 08/11/20]).
Principle of configurational sign-stimuli: picking out visual key features
Static and dynamic configurations
Sign-stimuli can be simple, such as vibration or bodily touch, suitable to elicit escape in a crayfish, or more complex. For example, configurational stimuli are determined by several features. Depending on the way features are related to each other, Tinbergen (1951) distinguished a static configuration (involving spatial relationships) from a dynamic configuration (involving spatiotemporal relationships, such as motion).
An example of static configuration is the sign-stimulus eliciting gaping in nestling thrushes, Turdus merula, toward the parent. In experiments using dummies (Figure 2.3b), the parent was modeled by two solid disks of different diameters, the large one simulating its rump r, the smaller one its head h. Nestlings aimed at the head, if the head-to-rump ratio was 1:3. This was examined with a “two-head-rump” model giving nestlings a choice between a head in 1:2 ratio and an adjacent one in 1:3 (Tinbergen & Kuenen 1939; cit. Tinbergen 1951). Hence h and r are features; their spatial arrangement yields the configuration. Its recognition is invariant to a change in other stimulus parameters, e.g., in size—within limits—provided the 1:3 ratio is preserved. Although movement improved the efficacy, the spatial relationship between head and rump turned out to be the prominent sign.
An example of dynamic configuration concerns the goose/hawk discrimination. Tinbergen (1951) showed that a bird model (Figure 2.3c) elicited escape in young turkeys, Gallopavo meleagris, when the model was flown overhead with the short end and the wings leading, simulating the silhouette of an airborne bird of prey. But the same model flown with the long end leading, resembling a harmless goose-like bird, was ignored. Subsequent research has shown that this configurational discrimination resulted from stimulus-specific habituation discussed later in this chapter.
Are there comparable signs with threatening stimuli across species?
Common toads, Bufo bufo, interpret small elongated objects—a worm or millipede—as prey. Experimentally, it can be shown that a 2.5 × 40 mm stripe oriented parallel to the direction of its movement releases eager prey-catching (see Further Reading, Movie A2). The same stripe suddenly oriented crosswise to the direction of movement—in a split-second—leads the toad to “freeze.” That configuration signals threat. Prey-like again, the stripe immediately elicits strong prey-catching activity, etc. The discrimination of these dynamic configurational “opposite stimuli” is invariant to changes in movement direction (Figures 2.3d, 2.4a–d) and velocity. This phenomenon was also observed in terrestrial urodeles (Finkenstädt & Ewert 1983).
Interestingly, the mudskipper Periophthalmus barbarus, an amphibious fish (Burghagen in Kutschera et al. 2008), and the preying insect Sphodromantis lineola (Kral & Prete 2004; cit., 2004) respond to such test-stripes in the same way as toads. Toward the threat-configuration, mudskippers may even raise their dorsal fins, thus threatening back.
Generalizing, a configurational feature perceived as threat here, is a contrast-border aligned crosswise to the direction of its movement. Unlike earthworms, snakes—the “archenemies” of toads—reveal such visual cues during locomotion: elevating head, undulating sidling body. Faced with a snake (Figure 2.5a) or a dummy snake (Figure 2.5b) a toad keeps eye contact, stops locomotion, discharges skin poison glands, swells up, assumes a stiff-legged defensive stance, and, eventually, presents its head and back like a shield difficult for the snake to handle (Ewert & Traud 1979, cit. Ewert 1984).
Figure 2.5 (a) Common toad displaying anti-predator behavior toward a ring snake or (b) to a snake dummy. (Courtesy of R. Traud.) .
Threatening postures, as components of agonistic behavior, shown for stickleback (Figure 2.1A), perch (Heiligenberg et al. 1972), or great blue heron (Figure 2.1B), are widespread in the animal kingdom. The caterpillar of Hemeroplanes triptolemus, if attacked, displays a scaring snake-like posture that is disregarded as prey. If human divers encounter a shark, experts recommend assuming an erect posture that will not fit shark’s prey schema.
We are tempted to speculate that during human evolution, the upright gait had—inter alia—a bearing on emitting a threatening signal. Wagging the erected forefinger against somebody as threat gesture, we interpret as a ritualized behavior. In fact, the significance of signs of that kind was known phylogenetically for a long time, such as with the amphibian genera Bombina and Bufo that emerged in the Jurassic and Paleocene, respectively
