Orientation (Insects)

Orientation refers to the way in which organisms direct their course of movement—not to their body or positional orientation per se, although, if an organism is to aim its course, it must align its body’s long axis with its intended track. Although orientation maneuvers thus involve an organism’s orientation of body position, this article is concerned mainly with movements in location that range in scale from millimeters to thousands of kilometers. A minute parasitoid wasp may walk to a resource, such as a prospective host, only millimeters away. On the other hand, movements of insects also can cover considerable distances, such as the longdistance migration of several thousands of kilometers that is undertaken in autumn by monarch butterflies (Danaus plexipypus) flying from northeastern North America to their overwintering site in central Mexico. The mechanisms that insects and other organisms use to accomplish such feats are enormously variable. Moment-to-moment steering typically relies on simultaneous inputs from multiple sensory modalities, such as chemical cues, light, sound, and wind. Most organisms use some stored information about very recent encounters with these cues and the organism’s past position. In many parasitic and social Hymenoptera, learned information, including spatial maps and landmarks, play a crucial role in these insects “knowing” either where they have been or their destination.

CLASSIFICATION OF ORIENTATION

MANEUVERS

The modern system of categorizing orientation mechanisms by their forms of locomotion and their presumed sensory inputs dates to Fraenkel and Gunn’s The Orientation of Animals, first published in 1940. These authors’ classification of maneuvers relies on two distinctive patterns of movement. The first kind of maneuver is termed a kinesis (pl. kineses); it is defined as an undirected response in which the body’s long axis exhibits no consistent relationship to the direction of the stimulus and the direction of locomotion is random. If a gradient of stimulus intensity regulates either the frequency of turns or the amount of turning per unit of time, the reaction is termed a klinokinesis. If the gradient of stimulus intensity regulates either speed or the frequency of locomotion, then the reaction is termed an orthokinesis. Both kinds of kinesis require at a minimum one sensory detector to monitor stimulus intensity, although multiple detector systems (such as paired antennae, each with many receptors) are the norm. Randomly directed movement would seem to be an ineffective means for moving toward or away from a stimulus. Klinokinetic maneuvers can facilitate movement either toward or away from a stimulus gradient as illustrated in Fig. 1 where simply turning more frequently in bright light eventually results in motion by the organism away from the bright light.

FIGURE 1 Track that could be expected from a hypothetical animal that always changes its direction by 90° to the right at a rate that is dependent on light intensity. The animal starts at point O. Turns occur more frequently when the animal is in bright light. Because of this tendency, the path cd is longer than ab. Although this is a simplistic representation of a klinokinetic reaction (in reality, turns will vary in angle and may be random to the right or left), it nonetheless demonstrates how klinokinesis can result in an animal orienting along a shallow stimulus gradient.
The second kind of maneuver is called a taxis (pl. taxes); it is defined as a directed reaction in which the organism’s long body axis is aligned with the stimulus and movement is more or less directed toward or away from the stimulus. In klinotaxis, the organism has available two strategies for sampling the intensity of the stimulus. In transverse klinotaxis, the sampling occurs by moving the entire body or a part of it from side-to-side along the path. Alternatively, in longitudinal klinotaxis, the organism samples intensity successively along its path. Both forms of klinotaxis require only a single detector capable of measuring stimulus intensity, although multiple receptors are typical. A classic transverse klinotactic reaction is the movement of blow fly larvae (Lucilia) away from light (Fig. 2). A close examination of the movement of larvae along their path reveals that although their tracks are nearly straight, their heads move from side to side. A similar pattern is seen in ants following a pheromone trail (Fig. 3 ).
Tropotaxis, in contrast, relies on a paired detector system (such as the antennae); by balancing the stimulus intensity on the two sides of the organism, the heading can be aligned with a relatively steep stimulus gradient. Honey bee workers (Apis), for example, can center their body’s long axis between balanced inputs of odor to each antenna. Telotaxis is a “direct” form of orientation in which the stimulus intensity is processed by a receptor system that has an array of directionally sensitive receptors, so that setting of a course toward a stimulus involves the relatively simple navigational task of holding a certain part of the receptor array in alignment with the stimulus. Sometimes termed “goal orientation,” telotaxis is known only for orientation along a beam of light.
In klino-, tropo-, and telotactic reactions, the organism’s long body axis is aligned with the direction of the stimulus, such as a beam of light or a fairly steep gradient of odor. In menotaxis, orientation of the long body axis is at a fixed angle to the stimulus, and course setting is maintained by stimulation of the sensory apparatus in a manner similar to telotaxis. Menotaxis is commonly called “compass orientation,” and some still unresolved form of it is used by monarch butterflies to head toward their wintering grounds, and by honey bees in their dance language. A menotactic reaction also seems to be responsible for the attraction to lights seen in many moths and

FIGURE 2 Courses (viewed from above) of blowfly (Lucilia) larvae crawling away from a light source (arrows depict direction of horizontal rays of light). The three individual larvae recorded are denoted “A” through “C” in different colors, and the tracks taken in repeated trials are indicated by numbers. Individuals in “A” and “B” seemed to deviate to the left in some trials and to the right in others. The track of larva “C” is represented in more detail than in the other tracks, showing alternating right and left movements of the head. Although J. Loeb stated that larvae “move as though they were impaled on a ray of light which passed through their medial plane,” the larvae clearly have some variability in their paths. Based on the detailed head movements of the track of larva “C,” larvae seem to orient by transverse klinokinesis.
other nocturnal insects. The assumption is that moths normally fly a straightened-out path by using celestial cues as a menotactic guide. When they encounter an artificial point source of light, they attempt to maintain a relatively constant angle with respect to the fixed point of light as in menotaxis, but in doing so they inevitably spiral toward the light source. Such a spiral path is indeed seen in the approach of some noctural insects to a light.

CLASSIFICATION OF SENSORY INPUTS

In describing how organisms orient, it is common to create terms that combine the kinds of environmental cue used in orientation with the form of taxis or kinesis. Common prefixes used include anemo (wind), chemo (odor or taste), mechano (pressure), phono (sound), photo (light), rheo (water flow), and scoto (darkness). The Lucilia maggot moving away from light can be said, for example, to be navigating by a negative transverse photoklinokinesis. It is obvious that the seeming precision of this classification scheme makes for an unwieldy terminology. This deficiency was noted in 1984 by Bell and Carde, who highlighted the need for “more practical, functionally related terms” that are not “teleological, poorly defined, nonprobabil-istic and difficult to spell.” A related problem is that these terms tend to define the reactions so precisely that they can dictate the boundaries of experimental investigations, such that these may either neglect the integration of mechanisms or fail to consider mechanisms that do not fall within these constructs.

FIGURE 3 Trail following in worker ants (Lasiusfuliginonus) in relatively still air. The straight red line marks the centerline of an odor trail. The dotted blue line denotes the path of the ant. The ant in “A” swings right and left across the trail, presumably bringing one antenna to an area of discernibly lower concentration before turning in the opposite direction. In “B,” the ant’s left antenna has been removed and she overcorrects her course to the right. In “C,” the antennae were crossed and then glued, but the ant is able to orient along the trail, albeit with difficulty, aided partially by a light compass reaction.
These classifications also neglect the role of internally stored information. The system of taxes and kineses assumes that an animal steers its path entirely in reference to the position of the external stimuli. However, the maneuvers can involve some self-steering that is governed by stored information about the animal’s previous path as well. Such information can be classified as either idiothetic (i.e., information that is internally stored) or allothetic (i.e., information that is external, such as visual features of the environment). Kineses are, for example, clearly self-steered, whereas transverse and longitudinal klinokineses are partially self-steered, and menotaxis is not self-steered.

ALTERNATIVE CLASSIFICATIONS

“Attraction” and “aggregation” are often used to categorize orientation, but these terms describe end points of orientation and tell us little about the preceding maneuvers. Attraction and aggregation nonetheless remain widely used to describe the consequences of taxes and kineses. Pheromones, for example, are often labeled as attraction pheromones or aggregation pheromones.
In another approach to classifying orientation mechanisms, Jander emphasized the distinction between the two broad categories of information used in orientation: information that is based on immediate sensory processing (for extrinsic or “exokinetic” orientation) and information that is stored centrally (for intrinsic or “endokinetic” orientation). Information that is stored may be subdivided into memory and that which is genetically determined. Jander also stressed the importance of ecology in studying orientation, and so his other categories included positional orientation (either staying in place or exhibiting locomotion), object orientation (movements with respect to the spatial position of either resources or sources of stress), topographic or home-range orientation (learned spatial orientation), and geographic orientation (migration over considerable distances).
Bell disavowed the time-tested system of taxes and kineses in his 1991 synthesis of foraging behavior. In analyzing the vast literature on foraging movements, Bell advocated describing the kinds of loco-motory paths that were observed, the kinds of information available to mediate the motor output, and the presumed guidance system. Bell eschewed terming any of these maneuvers “taxis” or “kinesis.” Despite such attempts to devise a new terminology, however, the system of taxes and kineses is likely to remain prevalent for some time because no clear alternative has emerged.

ODOR-INDUCED OPTOMOTOR ANEMOTAXIS

Among the best-studied orientation systems are those that enable organisms to locate upwind resources by flying along a plume of odor to the odor’s source. Examples of such maneuvers include male moths flying over distances of hundreds and perhaps thousands of meters to a pheromone-releasing female, tsetse flies and mosquitoes flying over tens and perhaps hundreds of meters to a prospective vertebrate host, and parasitoid wasps flying over several meters to their intended host. All these reactions are mediated by odors that are released by the resource and form an odor plume as they are carried downwind. It is crucial to note that maneuvers cannot be governed by orienting to a gradient of odor. A gradient that would be sufficiently steep for such directional information exists only within a meter or less of the odor’s source. Instead, insects and other organisms orient by advancing upwind when they encounter an above-threshold concentration of the odor linked to the resource.
The nonintuitive mechanism permitting in-flight anemotaxis is the optomotor response. An organism immersed in air or water cannot discern the direction of the flow of these fluids by mechanosen-sory input, although it can use mechanosensory information to gauge its airspeed or water speed (i.e., its movement relative to the fluid flow). Instead, it detects its displacement relative to its ground position by literally seeing how the flow alters its path. For example, if an organism’s long body axis is aligned directly with the fluid flow and the organism is making progress along the plume, then the image directly below or above the organism flows from front to rear. If the organism is moving at an angle to the fluid flow, then the image flows obliquely across the eyes (Fig. 4).
Optomotor anemotaxis was first demonstrated experimentally in 1939 by John Kennedy, with the yellow fever mosquito, Aedes aegypti. Kennedy’s ingenious wind tunnel used a movable pattern, projected onto the tunnel’s floor, to manipulate the visual feedback a flying mosquito would experience. He was able to show that the upwind flight of females induced by carbon dioxide (the activating ingredient in human breath) was governed by the optomotor reaction. When the projected floor pattern was moved in the same direction as the airflow, mosquitoes decreased their airspeed, apparently perceiving by visual feedback from below that their airspeed had increased; conversely, when the image flow was reversed to the opposite direction, mosquitoes immediately increased their airspeed. Mosquitoes regulate their airspeed to maintain a relatively constant rate of longitudinal image flow. These simple manipulations verified that the mosquitoes’ perception of movement relative to their visual surroundings dictates their airspeed, rather than some form of mechanosensory feedback.

FIGURE 4 The relationship between a flying insect’s body heading and the track taken when flying at an angle to the wind. The vectors depict the wind direction and velocity and the fly’s direction and velocity along the track. The image flow the fly sees directly below has both longitudinal and transverse components, and therefore flows obliquely across the fly’s eyes. When the fly heads directly upwind, the image flow is entirely longitudinal, i.e., front to rear.
The task an insect faces in finding an upwind source of odor, however, is much more complicated than simply flying upwind when an appropriate odor is encountered. Because turbulent forces cause the plume to meander and undulate, the direction of the plume’s long axis is not always aligned with the upwind direction. Thus, an insect proceeding upwind often exits the plume. Thus many insects “lose” the plume and then “cast”; that is, they stop moving upwind and instead move back and forth lateral to the direction of wind flow. If they recontact the plume during such to-and-fro maneuvers, upwind flight may resume. A further difficultly is that turbulent forces fragment the plume’s internal structure. Plumes therefore have patchy distributions of odor, so that even within the plume’s overall boundaries, insects encounter filaments of odor interspersed with gaps of clean air. Filaments can be encountered many times a second; for moths, whenever the encounters with filaments of odor are frequent, say above 10 Hz, flight can be aimed rapidly upwind, but when the encounter rate falls below 5 Hz, the flight can exhibit a much more substantial crosswind component (Fig. 5).
Odor-induced, optomotor anemotaxis as used by flying insects exemplifies several points common to orientation mechanisms. Several kinds of input (here visual, mechanosensory, olfactory) and self-steering all contribute to course setting and motor output. It is the integration of information that allows organisms to set their course.
Several related situations illustrate the variations on this theme. A flying insect also can orient along a plume of odor for moderate distances by flying a course that is set upon takeoff. After detecting the odor, the insect gauges upwind direction by mechanoreceptors and takes off due upwind. This is called an “aim-and-shoot” reaction, and the straight-line course is maintained by using visual cues perceived

FIGURE 5 Top view of flight tracks of males of the moth Cadra cautella flying toward a source of a sex pheromone. The moth is traveling from left to right. The dots represent the moth’s position every 1/30th of a second. The blue line shows the time-averaged centerline of the plume. Track “A” shows the path of a moth after intercepting a single puff of pheromone. [Redrawn from Mafra-Neto and Carde (1994), Nature 369, 142-144.] About 200 ms after intercepting the puff, the male surges upwind briefly. Track “B” shows a male flying along a narrow ribbon plume of pheromone, sporadically encountering pheromone. Track “C” shows a male flying along a wide turbulent plume of pheromone, encountering many filaments of pheromone per second.
ahead to set the course. Flight continues as long as the insect remains in the plume. Tsetse flies (Glossina spp.) are thought sometimes to use aim-and-shoot upon takeoff, but other observations support a conventional optomotor anemotaxis maneuver during flight. Tsetse flies may shuttle between these two orientation strategies. Walking insects use a nonoptomotor version of anemotaxis. Upon detection of odor, the insect simply heads upwind, using simple mechanosensory input to determine wind direction.

CONCLUSION

Taxes and kineses remain the principal organizing system for understanding and investigating how insects and other organisms “know where to go.” Discovering how these maneuvers work—what information is extracted, how it is processed, and the nature of guidance systems—remains an active area of inquiry.