Abstract

Adult tiger beetles are considered obligate predators in terrestrial ecosystems and reportedly feed on a wide variety of invertebrates, especially insects. The relatively open habitat preference of tiger beetles coupled with large bulging eyes suggests that predatory and attack behavior is largely reliant on visual cues. Some species of tiger beetles are ambush predators that frequently change ambush sites. When changing an ambush site, the adult tiger beetle moves a distance that is approximately equal to or less than its field of vision. This effects a systematic and thorough search of the foraging area. Within the foraging areas, attack behavior in adult tiger beetles was evaluated with respect to stimuli of movement, size, and color of potential prey. Experimentally, observations of actual attack by tiger beetles on prey were notably lower in the absence of movement. The frequency of attack was also measured with respect to color of potential prey. This implies that both movement and color of potential prey have stimulatory effects on attack behavior in adult tiger beetles. However, target tracking by moving adult tiger beetles poses problems. Pursuit movements by the predator degrade the image contrast of the target prey. Tiger beetles pursue prey in nature with several sequences of interrupted running. To successfully track prey, adult tiger beetles use this stop-and-go method to relocalize continually moving prey within their field of vision.

Introduction

Adult tiger beetles (Coleoptera: Cicindelidae) are primarily predatory beetles that inhabit a wide variety of terrestrial ecosystems (Pearson 1985, Wilson 1978, Willis 1967). Tiger beetles belong to the sub-order Adephaga, and recognition in the field is attributed to their long, sickle-shaped mandibles, large and prominent eyes in a head wider than the thorax, often striking and contrasting patterns on the elytra, and long, cursorial legs (Pearson 1988, Wallis 1961). Tiger beetles bear striking similarities to the family Carabidae, and some authors recognize these groups as a single family (Borror et al. 1989, Wallis 1961).

This family of beetles is principally diurnal and individuals are readily observed in preferred open exposed habitats of sandy stretches, forest clearings and bare ground with sparse vegetation (Pearson 1985, Dreisig 1981).

These insects are carnivorous and adults will actively hunt, capture and purportedly eat a wide variety of live terrestrial arthropods (Pearson 1988, Wallis 1961). Prey items include: ants (Formicidae), which make up a considerable portion of their diet, acridid grasshoppers, gryllotalpid crickets, lepidopteran larvae, small beetles (Carabidae, Cantharidae, Elateridae, Chrysomelidae, Curculionidae), and Collembola (Acorn 1991, Dreisig 1981, LaRochelle 1974, Wallis 1961). They have also been observed to readily scavenge on randomly encountered dead invertebrates (Dreisig 1981, Wilson 1978), and the species Cicindela repanda has even been observed to scavenge on rotting sassafras fruit (Hill and Knisley 1992).

Structure of foraging habitat

The search for and pursuit of prey occurs over a two-dimensional plane (Gilbert 1997, Dreisig 1981). In these open habitats, prey can be visually detected and pursued from a distance (Bauer 1981). A number of tiger beetle species are known to pursue prey on modified versions of this two-dimensional plane, i.e., on steeply sloped banks or cliffs, by running from leaf to leaf in an arboreal setting, on tree trunks, and on floating vegetation in aquatic systems (Kippenhan 1994, Pearson 1988).

Such open two-dimensional surfaces may often be resource poor in terms of arthropod diversity and densities (Kaulbars and Freitag 1993). This is often the case on tracks and trails where tiger beetles may be encountered and readily observed in the field. Tiger beetles may therefore forage preferentially and randomly near the interface of the two-dimensional plane and the adjacent vegetation. By remaining near the interface, the visual field of the tiger beetle is somewhat compensated. However, encounters with prey are increased due to "spill over" from the vegetation into the two-dimensional plane. There, the prey is continuously renewed in the exposed habitat, occurring there by mostly by accident (Kaulbars and Freitag 1993, Dreisig 1981). It is assumed by Dreisig (1981) that numbers of prey are not hunted to depletion due to migration of prey into the foraging area. Also, tiger beetles are generalist predators; that is, they do not specialize on one type of prey, therefore depletion of prey is not of great significance (Dreisig 1981).

Many of the pursued species are capable of flight during escape or dispersal, but tiger beetles do not fly during prey pursuit (Gilbert 1997). This enables the prey to successfully leave the plane of pursuit and to therefore avoid predation.

Optimizing and exploiting foraging conditions

Temperature is seen as the major determinant of the functional response of foraging (Dreisig 1981), so that prey density and success in locating prey is dependent on ambient temperatures, as is characteristic of poikilothermic individuals. However, poikilothermic as they are, tiger beetles can behaviorally regulate their body temperatures (behavioral thermoregulation) in such a manner that increases their encounters with prey items (Dreisig 1981).

Dreisig (1981) asserts that the ambient temperature level may serve as a cue in controlling the rate of foraging, to exploit the highest amount of prey items possible. Cicindela hybrida spends the inactive period of 24 hours in soil or sand burrows, and are induced to emerge from their burrows at a mean surface temperature of about 28ºC (Dreisig 1981). This threshold temperature for emergence occurs before that of the threshold emergence temperature for many prey items. During the low emergence temperature the tiger beetle does not actively forage; rather it basks in the sun to elevate its body temperature. By the time the tiger beetle reaches a body temperature that enables activity, the prey items begin to appear within the foraging area.

As the temperature rises, more time is used for prey searching and less for basking. The tiger beetle then will forage actively on randomly encountered prey items. It is probable that the number of prey increases as ambient temperature increases (Dreisig 1981). Generally, insect activity increases as the temperature increases, but only to a certain point, after which avoidance of the area occurs by smaller prey, because extremely high temperatures result in less favorable conditions of insect activity.

Dreisig (1981) describes prey exploitation through behavioral thermoregulation. When a sublethal body temperature of 35ºC is reached, the tiger beetle will raise its body away from the hot surface (stilting) to maintain its body temperature and continue foraging. Smaller prey, perhaps, do not possess the longer legs to effect this stilting behavior, and hapless individuals not successfully escaping hot surface temperatures are effectively trapped in the foraging area and therefore are more prone to predation by the tiger beetle. However, the tiger beetles remain active after the prey items have escaped the heat, but then will too later disappear by digging into the sand when the surface reaches an intolerable temperature of 44ºC. Therefore, through thermoregulatory activity, the tiger beetle can successfully exploit the entire period during which prey items are the most active.

Prey searching mechanisms

The combination of tiger beetles' preference for relatively open habitat, their diurnal pattern of activity, and their large bulging eyes suggests that predatory and attack behavior is largely reliant on visual cues (Pearson 1985, Bauer 1981, Wilson 1978), although several tiger beetles in the genus Cicindela do possess tympanic membranes that are sensitive to airborne sounds (Spangler 1988). Another genus, Megacephala, is known to possess a modified version of this hearing organ (Spangler 1988), and at least one nocturnally active species, Megacephala fulgida, is known to phonotaxically locate mole crickets for prey (Fowler 1987).

Cursorial species as they are, tiger beetles observed in the field by Nachtigall (1996) were noted to scan the forage area by running quickly for short distances, then brake, then abruptly accelerate, and then stand motionless for a few seconds. They would then continue running in the predisposed direction, or abruptly turn on the spot and head in another direction. Tiger beetles do not choose a single foraging area; rather they move discontinuously from spot to spot (Kaulbars and Freitag 1993), and it is assumed that the predator searches randomly over its plane for the prey (Dreisig 1981). This effects a systematic and thorough search of the foraging area. A tiger beetle searches in a more or less straight path for a few meters and then suddenly will randomly change its course (Dreisig 1981). During these discontinuous movements, a tiger beetle will pause in each location for a time, which ranges from several seconds to several minutes (Kaulbars and Freitag 1993).

Kaulbars and Freitag (1993) observed that the random foraging pattern of the beetle is such that by moving frequently and randomly, it will successfully locate prey items over time. Following the capture of prey, an area-concentrated search effort does not commence, but rather the random search is continued (Dreisig 1981). As noted previously, ants are a common food item of tiger beetles (Willis 1967). Where an ant is encountered increases the likelihood that more will be encountered in the vicinity. Continuing its random search in an area of high prey concentration (i.e., ant colonies) will result in the tiger beetle remaining for a longer period of time in the area of the prey concentration and result in an exploitation of the prey source (Kaulbars and Freitag 1993, Dreisig 1981).

Cues, detection, and pursuit of prey

Mobile prey is detected visually from a distance of approximately 16-25 cm and will typically trigger a four-stage reaction (Lovari et al. 1992): 1) a change in the body position from a horizontal pose to that of a steeply inclined alert posture; 2) orientation of the long axis of the tiger beetle's body towards the visual stimulus, followed by an actual attack, which consists of quick runs interrupted by short pauses; 3) the bite and the capture; and 4) devouring of prey.

Prey size and especially prey movement are two factors that are very significant in eliciting a predatory response (Lovari et al. 1992). Other factors that may contribute to the predatory response are shape of the prey, contrast of color (dark objects on a light background), as well as memory of prey shape and location (Fausch 1968).

Lovari et al. (1992), through experimental use of dummy baits of six colors (red, brown, black, green, blue, white) and varying sizes (3.8, 7.5, 15, 30 mm), demonstrated that visual cues of certain sizes and colors will trigger predatory response in the tiger beetle species Cephalota circumdata leonschaeferi. One phase of this experiment used baits of varying colors without movement. This phase resulted in only 20 attacks out of 522 tests (3.83%) on the baits, with red baits scoring the most attacks and white the least. Using a combination of movement, size and color, Lovari et al. (1992) observed that attacks on baits about 7.5 mm in size in combination with red color elicited the most attacks. This same size in combination with black or brown elicited similar attack responses. Attacks were also observed on bait sizes of 3.8 and 15 mm, but a large sized bait of 30 mm was avoided. The avoidance of the large bait could be explained in terms of attempts by a predator to overcome prey larger than itself is energy expensive and extremely risky, and therefore not adaptive (Lovari et al. 1992).

This preference for the red bait was difficult to explain because most available prey items in the natural setting, although of differing colors, are not red. It is necessary to explain this preference for red in terms of the habitat were the observations took place (Lovari et al. 1992). Apparently, the habitat was an alkaline salt flat, very pale in color, and red was the bait that most strongly contrasted with the substrate, therefore facilitating visual definition, which in turn may facilitate item localization by the tiger beetle (Lovari et al. 1992). Apparently, the whiter or less contrasting colors in this habitat do not contrast enough with the substrate to elicit a predatory response.

The perceptual field of the tiger beetle will vary depending on the size of the prey, the contrast of the prey with its substrate, and probably on some other unknown factors (Dreisig 1981). Dreisig (1981) estimated that the species Cicindela hybrida, detects bigger prey (spiders and beetles) from a distance of about 30 cm while smaller ants were detected visually at 10 to 15 cm. Dead insects apparently required the closest range of detection, about 7-10 cm, and were usually detected through tactile stimulation during random searches. Dead or non mobile prey have absence of movement, and apparently movement is necessary to elicit a predatory response from a distance.

When a tiger beetle detects prey, it will orient towards it, rush it, and then attempt to seize it with its mandibles (Dreisig 1981). Successful predation of the prey depends on its size and the nature of the prey, and one of the following modes of actions may take place (Dreisig 1981): 1) the tiger beetle may realize that the prey is immune to attack (i.e., ants that spray deterrents at attackers, or prey that is very large), and will release the item and run away; 2) the item of attack may be quite large, and repeated lunges at the prey item are followed by bites that eventually overcome the large prey, which is then torn to pieces and eaten; or 3) the item of attack is small, and the tiger beetle then begins to chew immediately. When the prey is swallowed, the tiger beetle searches for any leftover edible fragments, and then resumes its usual random search behavior.

Success of overcoming prey varies for several reasons that follow (Dreisig 1981, Wilson 1978). The prey may be overlooked, perhaps because movement in the prey item is lacking, and therefore does not transmit the threshold degree of movement that is necessary for detection by the tiger beetle. Vegetation in the plane of forage may obstruct the view of the prey item, so the possibility of overcoming the prey then becomes very small, as tiger beetles forage very inefficiently in the presence of vegetation. Some prey species, especially ants, will exploit vegetative cover to obscure their presence from the predator. Also, a "waiting game" will often ensue. When a prey species detects a predator's approach, it will freeze, and remain motionless. Since attack is largely reliant on movement by the prey item, the tiger beetle cannot relocate the prey item, and will return to its random search method. These waiting games are interesting because they do not involve any particular structure on the part of the predator or prey to determine who "loses" (Wilson 1978), rather, it is behavioral. Whoever can wait the longest will usually win the game. The cost is the loss of time, and the outcome of who wins or loses is selectively more important for the prey (where the risk equals injury or death), than for the predator (the risk of a lost meal) (Wilson 1978).

Visual localization of prey and success in capture of prey

Movement of the prey to visually trigger a predatory response is strongly suggested throughout (Wilson 1978). The foraging area of the tiger beetle is limited to a circle that is the extent of the beetle's vision, and when foraging from site to site, the adult tiger beetle moves a distance that is approximately equal to or less than its field of vision (Kaulbars and Freitag 1993). This circle of vision varies among species. For example, it is estimated for C. purpurea to be 8-13 cm (Moore 1906) and 25 cm for C. hybrida (Swiecimski 1957).

The response of the beetle to movement, as is characteristic for visually hunting insects, is to turn its medial sagittal plane toward the location of the movement (Bauer 1981). Subsequent movements by the prey item elicit a brief approach response (Bauer 1981). Each approach is variable, but the length of approach is shorter as the prey is approximated (Bauer 1981). Immediately prior to attack, the beetle probably fixates on the site where the contrast of the prey against its substrate is the greatest (Bauer 1981). Should the prey move at this phase, the beetle will compensate by repositioning its midline and approach again until the critical attack distance is again reached (Bauer 1981).

While in motion during foraging, tiger beetles make many short pauses, presumably in search of prey (Gilbert 1997, Kaulbars and Freitag 1993). During an attack phase, the beetle also makes short pauses during pursuit, albeit at smaller intervals (Gilbert 1997). For a visual, rapid cursorial predator to constantly make stops while in pursuit of prey is somewhat odd, because if a predator uses vision to continually track prey while in pursuit, no stops should be made (Gilbert 1997). This stopping behavior may indicate that the predator has temporarily lost track of its prey, and must stop to relocalize the prey in order to continue its pursuit (Gilbert 1997). It is here during these relocalization stops that the "waiting game" described earlier (Wilson 1978) is played out. If the prey freezes, through absence of movement, no visual stimulus required by the predator occurs, and instead of continuing, the tiger beetle will abandon its pursuit and begin its random forage pattern again (Gilbert 1997).

Target detection of prey, however, poses problems for mobile predators that rely on vision to detect prey (Gilbert 1997). In high-speed maneuvers, insects can run, rotate, and turn up to hundreds of degrees per second, so blurring of images while running becomes a real challenge to overcome (Land 1997). The problem lies within the compound eye of the insect predator (Land 1997). Each ommatidium in a compound eye has its own lens, and because there are a large number of lenses, they must be small (Land 1997). The resolution of these lenses is limited by diffraction, something that also limits the resolving power of microscopes and telescopes (Land 1997). The resolution of each lens of the insect compound eye, therefore is about 1º, or one hundredth that of the human eye, which has a larger aperture (Land 1997). Interestingly enough, if the compound eye were given the same resolution as a human eye, one eye would have the radius of 6 m (Land 1997). Therefore, visual acuity for the tiger beetles here is very limited, with detection of large prey first occurring from a distance of 25 to 30 mm.

Analysis through filming pursuit of prey or of experimentally controlled dummies by Gilbert (1997) discerned that adult tiger beetles use visual angular velocity and position of prey as a cue to narrow in, converge with, and successfully effect capture of prey. Gilbert (1997) suggests that the tiger beetle, in its natural setting, is using an "open-loop" behavioral mechanism to track prey, that is, the tiger beetle initially localizes the prey, and runs in the direction to where the prey was last located. Apparently, a threshold stimulus of two ommatidial fields must be reached before a predatory response is triggered (Gilbert 1997), and it is evident that during pursuit the beetle views the prey with the part of its eye where its vision is most acute, in the large pseudopupil (Bauer 1981). However, during this initial run by the predator, the prey has moved. The tiger beetle, now pausing in the location where it last aimed to run, relocalizes the prey and sequentially heads in the next direction. Finally, at the last and shortest pursuit, the prey is overcome by the tiger beetle and successfully caught. Apparently, this open loop behavior is also in use during the tiger beetle's search in the foraging area described by Kaulbars and Freitag (1993), explaining the constant stop-and-go iterations that are observed during random foraging. Hence, proximal prey with movement, within the parameters of an easily defeated size, and with contrasting color in relation to that of the substrate, all serve as cues to facilitate localization and capture of the prey by the tiger beetle.

LITERATURE CITED