The Mimetic Flight Behavior of Hoverflies

Most examples of mimetic insects occur in the tropics, but temperate Europe and United States. are home to many species of hoverflies (Diptera: Syrphidae) that are thought to be Batesian mimics of wasps and bees [28,77]. Some are black and yellow or red, resembling social and solitary wasps; others are large and hairy, resembling bumblebees (some are polymorphic, mimicking different species); while others, notably droneflies of the genus Eristalis, resemble honeybees. Some hoverfly mimics appear to closely resemble their models in morphology, while others are only superficially similar. Dipterans and hymenopterans, although both flying insects, have quite different ecologies; hymenopterans are often social insects that forage on flowers for nectar and pollen for the colony, or in the case of solitary species, for provisioning their nest. Hoverflies are always solitary animals that do not exhibit parental care. However, both spend much of their time foraging on flowers, during which time they are particularly obvious and vulnerable to predation by birds [78]. In a study of foraging behavior, Golding and Edmunds [53] found that droneflies often spent a similar amount of time as their honeybee models, both feeding on individual flowers and flying between them, when foraging on the same patch. Because they are seeking different rewards from the flowers and in different quantities, the most likely explanation is that this is a case of behavioral mimicry; the hoverflies, which are unprotected insects, are adapting their behavior to appear more like their model hymenopterans.

There have also been many suggestions that hoverflies show flight mimicry of hymenopterans. Different species have been referred to anecdotally as having beelike flight [13], bumblebeelike flight [79], and lazy wasplike flight [80]. One of us (Golding) has also observed the hoverfly Xanthogramma pedissequum, a black and yellow wasp mimic, adopting an uncharacteristic flight behavior; it flew about 30 cm above low-growing vegetation in a zigzag fashion very similar to the behavior of a hunting wasp (personal observation). Morgan and Heinrich [81] observed that the mimicry of many of the hoverflies they studied appeared most accurate in flight. They also showed that hoverflies (including Eristalis) were able to warm up using behavior such as basking or shivering, which they suggested might allow them to behave more like their endothermic models. There have been few studies, however, that have empirically measured or formatively studied these behaviors, even though the flights of hoverflies and bees have both been well studied.

The aerodynamics of both groups has been elegantly elucidated by Ellington [68]; the flight mechanism, wing design, and kinematics of hoverflies has been investigated by Ennos [82-84]; and other behavioral aspects, such as the mechanism by which hoverflies compute interception courses and manage to return to exactly the same spot, have been studied by Collett and Land [85,86]. Any flight mimicry between the two groups must be quite unlike the locomotor mimicry between butterflies. For a start, the warning coloration of Hymenoptera and their hoverfly mimics is displayed on the abdomen and thorax, not the wings. Second, the flight apparatus of hoverflies and Hymenoptera are quite different. Hoverflies have two wings and twist them on the upstroke in the manner described by Ennos [83]. In contrast, the Hymenoptera have four coupled wings, with positive camber at the base, which are twisted in the upstroke by the same mechanism as in butterflies [87] (personal observation). Therefore there is no possibility of convergence in their mechanics. Furthermore, convergence in wingbeat frequency cannot be involved in the mimesis because the wingbeat frequency of both groups is far too high at 150 to 250 Hz for predatory birds to detect or even for them to be able to see the wings in flight. These wingbeat frequencies also overlap extensively with each other and with those of other insects that use asynchronous muscles [68,84,88].

Hoverflies are generally regarded as having superior flight agility compared with hymenopterans because their center of body mass (CMbody) is closer to their wing base [68]; they use inclined stroke plane hovering; and they have the apparent ability to move the aerodynamic force vector independently of the stroke plane [84]. Therefore one would expect any flight mimicry to involve the body movements of the insects, not the wings, and that hoverflies would have to compromise their flight ability when foraging to appear more like a hymenopteran.

In the first quantitative study of flight mimicry in the group, Golding et al. [54] examined the flight of hoverflies of the genus Eristalis, which are known as droneflies and are considered to be Batesian mimics of honeybees (Apis mellifera). They are of similar overall shape and body mass, although female Eristalis spp. tend to be slightly larger than males. In appearance droneflies differ from honeybees in having shorter antennae, no discernable "waist," one pair of wings, and often more orange or yellow markings on the abdomen. Filming from above a patch of flowers in the field, Golding measured the horizontal flight velocities and routes taken by insects free flying between individual flowers when foraging. She compared E. tenax with A. mellifera along with a control hoverfly (Syrphus ribesii) and a nonmimetic muscid fly. It was found that droneflies did indeed show more similar flight movements to the honeybee than to the other two insects [54]. The muscid flew faster than the other three species and took more direct routes between flowers. The control hoverfly flew at similar speeds to the dronefly and honeybee, but took longer to fly between the flowers because it took more convoluted routes and hovered more. The dronefly flew at similar speeds to the honeybee, took similarly convoluted routes, and hovered for similar amounts of time.

The dronefly also performed loops along the flight path similar to those performed by the honeybee. This behavior was not detectable to the human eye, but it may well be to a predatory bird because they can detect motion two to four times faster than humans [76]. The looped flight of honeybees may be connected with their ability to orientate their position in relation to the hive using the sun, as described by von Frisch [89]. It is surprising behavior for droneflies, however, as they are capable of sudden changes of direction without altering their body position; they can perform turns of over 90 degrees while traveling less than one body length [68,84]. The most likely explanation of the looping flight of foraging droneflies is that their flight behavior has been modified to be more similar to that of their hymenopteran model. This cannot be classed as locomotory mimicry as defined by Srygley [70] in his studies of more closely related butterflies because the organisms have such different flight apparatus, but it could accurately be described as mimetic flight behavior. Closer examination of these maneuvers using high speed cinematography might help determine whether the aerodynamic mechanisms used by the two species are the same. However, the droneflies have still retained the ability for fast accurate flight to escape predation and in males for patrolling territory and chasing females.

Golding et. al. (in preparation) are continuing with this work on other mimicry groups. The most recent results are from a study of flights between flowers made by social wasps (Vespula vulgaris) and four of their hoverfly mimics (Sericomyia silentis; Myathropa florea, Helophilus pendulus, and Syrphus ribesii). Sericomyia silentis is a large fly similar in size to V. vulgaris, and they occur together during late summer; Sericomyia silentis is a conspicuous, bright yellow and black species. The other three yellow and black species are smaller than wasps but are similar in size to each other although M. florea can be slightly larger. H. pendulus and M. florea have more elaborate markings, both on thorax and abdomen than Syrphus ribesii. To the human eye, Sericomyia silentis appears to be the best mimic and Syrphus ribesii, the poorest with H. pendulus and M. florae midway between the two. It might be expected therefore that Sericomyia silentis would show the most similar behavior to its hymenopteran model. In contrast, preliminary results from analysis of 115 flights performed by 53 individuals from the 5 species seem to be showing the opposite. Syrphus ribesii flies at similar speeds to wasps and has comparable flight trajectories; it takes similar, more convoluted routes as wasps and flies relatively slowly between flowers. Sericomyia silentis, M. florae, and H. pen-dulus have similar speeds and flight trajectories to each other; they fly straighter and faster (Figure 10.1).

An interpretation of these results is that Syrphus ribesii has to compensate for its poor morphological mimicry by showing better behavioral mimicry. It adopts

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