The Mimetic Flight Behavior of Butterflies

Much of the modern work on flight mimicry in tropical butterflies has been carried out in Central America starting with Chai's [22] study of butterfly predation by the specialist feeder, the rufous-tailed jacamar (Galbula ruficauda). These birds feed exclusively on flying insects; in fact, they do not recognize prey that does not fly. Chai established that captive jacamars fed on a wide range of butterflies and that they could distinguish between palatable species (Papilio; Morpho; Charaxinae; Brassolinae; Satyrinae and most Nymphalinae) and the unpalatable species (Battus and Parides [Papilionidae]; Diathreia and Callicore [Nymphalinae]; Heliconiinae; Acraeinae; Ithomiinae; Danainae and some Pieridae), most of which were members of Mullerian mimicry groups. Most of these were sight rejected. The birds were so adept that they could even distinguish between the very similar color patterns of some Batesian mimics and their models, although some mimics such as Papilio anchisiades were never taken by jacamars in feeding trials. Chai suggested that the birds made these assessments based both on the warning coloration on the wings and on the flight behavior of the butterflies. He stated that many unpalatable butterflies flew with "slow and fluttering wingbeats" and in a "regular path" that would enable them to display their warning colors. The flight of the Batesian mimics was described as being similar to that of their models, whereas other palatable butterflies flew faster and more erratically, making them harder to catch. Importantly, Chai established that jacamars could memorize the palatability of a large variety of butterflies, suggesting that insectivorous birds, such as jacamars, were likely to play a major role in the evolution of neotropical butterfly mimicry. Interestingly, Kassarov [61] suggested that the aerial hawking birds recognize butterflies by their flight pattern rather than by details of aposematic or mimetic coloration. Evidence has been presented that insectivorous birds can perceive motion two to four times faster than humans [62]; they also have superior color vision and are able to detect UV markings that humans cannot see [63].

The qualitative flight observations were later backed up by more quantitative studies of the flight behavior, body temperature, and body morphology of the butterflies [64-66]. Unpalatable Mullerian species did indeed fly more slowly and more regularly than palatable species when filmed flying in an insectary [64]. They were also able to fly at lower ambient temperatures and had lower thoracic temperatures when caught. Srygley and Chai [65] suggested that these differences could also be related to the contrasting body morphology of the two groups. The palatable, fast-flying butterflies had relatively wider thoraxes that could house the more massive flight muscles they would need for fast speed flight and rapid acceleration. To achieve this, however, they would have to have higher thoracic temperatures and so would be restricted to flying in warmer ambient temperatures. In contrast the unpalatable butterflies, with their slower, more economical flight, could fly at lower temperatures and divert more of their resources into a larger abdomen. This idea is incompatible, however, with a later idea of Srygley [67] about noncheatable signals. Here he suggested that flight mimicry might actually impose an aerodynamic cost, so that Mullerian and Batesian mimics would need to develop more power to fly than palatable butterflies. To test this idea, Srygley analyzed films of the flight of two species of palatable butterfly, four species of Mullerian mimics, and two Batesian mimics, and calculated the power required using the quasisteady analysis method of Ellington [68]. The Batesian mimics did have higher weight-specific power, but the power requirements of the other two groups showed extensive overlap. Theoretically, it seems unlikely in any case that an unpalatable butterfly would choose to fly in an uneconomical way. The matter is complicated because butterflies, like other insects, make extensive use of nonsteady aerodynamics [69], which will affect their power requirements. Clearly more research using additional species and examining the actual oxygen uptake of the insects rather than modeling the power is needed to settle this matter.

The morphological differences between palatable and unpalatable butterflies and their consequences were later examined in more detail [66,70]. These studies showed that in unpalatable Mullerian mimics, the wing center of mass was further from the body and the center of mass of the body was further behind the base of the wings than in palatable species. Both of these would make the insect less maneuverable, but give it smoother flight because of the increased moment of inertia [68], whereas the reverse was true for the palatable species. Srygley [10,70] therefore suggested that similarities in morphology in these insects lead almost automatically to "locomotor" mimicry in which "adaptive convergence of physiological and morphological features result in similar flight biomechanics and behaviour." In the Batesian mimic Consul fabius, although the center of mass of the wing was far from the body, as in the unpalatable Mullerian mimics, the center of mass of the body was near the wing base, as in other palatable species. Srygley [70] suggested that this intermediate morphology would enable this butterfly to fly rapidly and unpredictably if disturbed, like other palatable species, so it could escape if its mimicry proved unsuccessful.

In this context, it is interesting that the majority of Batesian mimetic butterflies are female [1,71], which typically have larger abdomens for the development of eggs and, as a consequence, relatively smaller thoraxes than males [64,72]. This would make them less maneuverable and hence more vulnerable to predation [55]. Since females are also longer-lived, there would thus be strong selection pressure for them to evolve the warning coloration of unpalatable butterflies to gain greater protection from birds. Females would also be more easily able to adopt the slow, regular flight of these species. Confirming this supposition, Ohsaki [73] found that in general female butterflies were attacked more frequently than males but that Batesian mimetic females (protected by their mimicry), males (protected by fast erratic flight if palatable), and the unpalatable models were attacked less than nonmimetic females. Ohsaki suggested that when the predation by avian predators is female biased, female-limited mimicry will be favored even if the costs of mimicry are the same for both sexes. The case is different in Mullerian mimicry in which unpalatable species resemble each other; all individuals of both sexes will usually become mimetic.

The locomotor mimicry that Srygley described has been most clearly demonstrated in studies of the flight kinematics of four mimetic butterflies of the genus Heliconius [74-76]. These make up two Mullerian mimicry pairs in which each species is more closely related to a member of the other mimicry pair than to the insect it mimics. Using multivariate statistics, Srygley [76] was able to separate the effects of evolutionary convergence from those of phylogeny. It was found that the mimics were more similar to each other than to the other closely related species in their wing-beat frequency, the degree of asymmetry in wing motion, and in their transport costs. It has been suggested that this is the first clear example of a mimetic behavioral signal for a flying insect [74-76]. However, since the morphological mimetic signal is displayed by the organs of locomotion, the wings, it might in any case be expected that flight mimicry would occur if the wings showed convergence in form; this would greatly constrain the kinematics and aerodynamics. It should also be emphasized that the research on flight mimicry in butterflies has been based on the analysis of a very few flights made often by only a single member of particular species. The films, moreover, are of captive individuals flying in artificial conditions. More film of free flight in the field might help show other more subtle aspects of flight mimicry and flight behavior.

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