world in which the organism lives. Jacob von Uexküll (1921) pointed out that each animal species lives in, and communicates with, its own sensory world, the “Umwelt.” Different species perceive their Umwelt differently, and quite differently from the way we humans perceive our environment. Knowledge about the capabilities of sense organs indicates the kinds of stimuli perceived by organisms and suggests what their perceptual worlds look like (Prete 2004).
Certain species have evolved perceptual talents. In birds, visual acuity and accommodation speed of the eyes are maximized at 20/4 vision, compared to 20/20 in humans. From high altitudes raptors can magnify and detect small prey on the ground while monitoring a wide field of vision. Many insects—like some birds—are sensitive to ultraviolet light and may use polarized skylight for navigation (Labhart & Meyer 2002). Barn owls, Tyto alba, hunting in darkness, localize sound sources by tiny interaural time differences (Konishi 2003) (Chapter 5). Dogs and mice live mainly in a world of smell, spiders in a world of vibration. Rattlesnakes, Crotalus viridis, have infrared-sensitive pit organs for object detection in the dark (Newman & Hartline 1982). Dolphins and nocturnal bats use biosonar (Suga 1990), and weakly electric fish produce electric fields for object detection and communication (Heiligenberg & Rose 1985). Sharks utilize electroreceptors to detect electric fields of about 0.005 μV/cm, e.g., from breathing-muscle potentials by a flatfish hidden in the sand. Like migratory birds, loggerhead turtles, Caretta, detect geomagnetic cues that vary across the earth’s surface and employ magnetic-compass orientation for long-distance navigation (Wiltschko & Wiltschko 2002).
Male silk moths, Bombyx mori, are “smell champions.” One molecule of the female’s sex attractant pheromone bombykol is sufficient to elicit a nerve impulse in a receptor cell specialized for bombykol (Kaissling 2014). The female’s pheromone glands contain less than 1 µg bombykol, which, theoretically, is sufficient to lure 1013 Bombyx males. In males the behavioral olfactory threshold is 103 bombykol molecules/cm3 in an air stream at a velocity of about 50 cm/s. Actually, 200 simultaneous molecule hits at 200 of the more than 25,000 bombykol receptors tell the Bombyx male: a female is present in the direction from which the wind blows. For comparison, in German shepherd dogs the behavioral threshold for butyric acid, a component of sweat, is 5.9×103 molecules/cm3.
Whichever type of energy the receptor cells respond to—odor, infrared, sonar, etc.—the corresponding sensory systems have a comparable basic structure: receptor cells and nerve cells connected to them. Perception involves the neurosensory as well as the motivation and attention related processes, by which an organism becomes aware of and localizes and recognizes external stimuli.
A few comments on stimulus recognition are appropriate. Recognition (identification, interpretation, detection) in the present context means that stimuli from the environment are classified into meaningful units, i.e., categories of functional (behavioral) significance. A category can be a class of behaviorally significant objects that approximately share a set of defining features. Approximate, rather than specific, is the suitable term, since it enables “openness” in category formation. How organisms sort objects into different categories according to features is one of the basic questions in the behavioral and cognitive sciences. The problem is general, as an “object” can be any recurring signal (associated with experience or species-specific knowledge) and “sorting” is related to any differential response to it. Categorization—the ways that categorize information—plays a critical role in perception, thinking, and language (see Harnad 1987).
Sign Stimuli
Stimulus perception in male sticklebacks
To understand how an animal interprets a stimulus means investigating how the animal responds to it. In his famous textbook The Study of Instinct, Tinbergen (1951) introduced the topic of stimulus perception with an experiment (Figure 2.1A):
Figure 2.1 (A) The “reflection experiment.” Toward its mirror-image a male stickleback assumes a vertical threat posture. (Abstracted after a photo in Tinbergen 1951). (B) Great blue heron, Ardea herodias, in threat-display: bill/neck vertically straightened. (Abstracted after a photo in: http://redandthepeanut.blogspot.de/2010/06/two-great-blue-herons-face-off-in.html [accessed: 08/11/20]).
A male three-spined stickleback, Gasterosteus aculeatus, seeing its reflection in a mirror, assumes a vertically oriented body posture with the head pointing downward.
Tinbergen listed a set of issues that must be addressed in order to answer why, in a causal sense (Chapter 1), the animal does this. These questions concern the processes hidden in a “black-box” that, so to speak, translates the stimulus into the behavioral reaction (Figure 2.2).
Figure 2.2 Looking into a “black-box”: principles of brain function mediating between sensory input and motor output. (Modified after Ewert 1976).
First, we must classify the reaction in a behavioral context (e.g., reproduction, male–male aggression). The fact that a male stickleback in reproductive state shows this behavior suggests the involvement of hormones, which requires neurochemical investigations. Then we should examine the releasing features of the visual stimulus and analyze the neuronal instruments that extract the features, exploring the processes responsible for stimulus recognition and localization. Furthermore, the releasing value of a stimulus may depend on motivation and experience. The information regarding stimulus features, locus, memory, attention, and motivation yields a releasing mechanism that activates motor pattern generation responsible for eliciting the adequate behavior. What Tinbergen is suggesting is that “neural orchestration” in the whole brain participates in what appears, initially at least, as a relatively simple stimulus–response.
Back to the “reflection experiment” (Figure 2.1A): what is the ethological background? A male stickleback encountering a conspecific male in its territory changes its longitudinal body axis into a vertical head-down position, thus signaling threat. In fact, when placing a male into a narrow glass tube (Figure 2.3a), the responses of territorial males were stronger when the tube was oriented vertically compared with when the tube was oriented horizontally (Ter Pelkwijk & Tinbergen 1937; cited in Tinbergen 1951). Furthermore, the red coloration of the male’s belly contributed to the release of aggressive attacks. Strongest responses were obtained when both features—vertical posture and red color—occurred together. Later, Heiligenberg et al. (1972) demonstrated quantitatively in the male perch, Haplochromis burtoni, that its black eye-bar delivered a threat-signal to conspecific males that, too, was enhanced if the fish assumed a vertical head-down posture.
Figure 2.3 Configurational features in sign-stimuli. (a) Three-spined stickleback, in a glass tube, in threat posture and prevented from assuming a threat posture. (Ter Pelkwijk & Tinbergen 1937.) (b) Parent thrushes simulated by a head(h)/rump(r) model. Nestling’s gaping (arrow) is directed toward parent’s head. (Tinbergen & Kuenen 1939.) (c) A bird model moving overhead turkeys resembles a goose-like bird or a hawk, depending on the movement direction. (Tinbergen 1948; cit. 1951) (d) A moving
