Adrian Vallin

Prey survival by predator intimidation: an experimental study of peacock butterfly defence against blue tits

Long-lived butterflies that hibernate as adults are expected to have well-developed antipredation devices as a result of their long exposure to natural enemies. The peacock butterfly, Inachis io, for instance, is a cryptic leaf mimic when resting, but shifts to active defence when disturbed, performing a repeated sequence of movements exposing major eyespots on the wings accompanied by a hissing noise. We studied the effect of visual and auditory defence by staging experiments in which wild-caught blue tits, Parus caeruleus, were presented with one of six kinds of experimentally manipulated living peacock butterflies as follows: butterflies with eyespots painted over and their controls (painted on another part of the wing), butterflies with their sound production aborted (small part of wings removed) and their controls, and butterflies with eyespots painted over and sound production aborted and their controls. The results showed that eyespots alone, or in combination with sound, constituted an effective defence; only 1 out of 34 butterflies with intact eyespots was killed, whereas 13 out of 20 butterflies without eyespots were killed. The killed peacocks were eaten, indicating that they are not distasteful. Hence, intimidation by bluffing can be an efficient means of defence for an edible prey.

Marginal eyespots on butterfly wings deflect bird attacks under low light intensities with UV wavelengths

Background Predators preferentially attack vital body parts to avoid prey escape. Consequently, prey adaptations that make predators attack less crucial body parts are expected to evolve. Marginal eyespots on butterfly wings have long been thought to have this deflective, but hitherto undemonstrated function. Methodology/Principal Findings Here we report that a butterfly, Lopinga achine, with broad-spectrum reflective white scales in its marginal eyespot pupils deceives a generalist avian predator, the blue tit, to attack the marginal eyespots, but only under particular conditions—in our experiments, low light intensities with a prominent UV component. Under high light intensity conditions with a similar UV component, and at low light intensities without UV, blue tits directed attacks towards the butterfly head. Conclusions/Significance In nature, birds typically forage intensively at early dawn, when the light environment shifts to shorter wavelengths, and the contrast between the eyespot pupils and the background increases. Among butterflies, deflecting attacks is likely to be particularly important at dawn when low ambient temperatures make escape by flight impossible, and when insectivorous birds typically initiate another days search for food. Our finding that the deflective function of eyespots is highly dependent on the ambient light environment helps explain why previous attempts have provided little support for the deflective role of marginal eyespots, and we hypothesize that the mechanism that we have discovered in our experiments in a laboratory setting may function also in nature when birds forage on resting butterflies under low light intensities.

Magnetic cues and time of season affect fuel deposition in migratory thrush nightingales (Luscinia luscinia)

Bird migration requires high energy expenditure, and long–distance migrants accumulate fat for use as fuel during stopovers throughout their journey. Recent studies have shown that long–distance migratory birds, besides accumulating fat for use as fuel, also show adaptive phenotypic flexibility in several organs during migration. The migratory routes of many songbirds include stretches of sea and desert where fuelling is not possible. Large fuel loads increase flight costs and predation risk, therefore extensive fuelling should occur only immediately prior to crossing inhospitable zones. However, despite their crucial importance for the survival of migratory birds, both strategic refuelling decisions and variation in phenotypic flexibility during migration are not well understood. First–year thrush nightingales (Luscinia luscinia) caught in the early phase of the onset of autumn migration in southeast Sweden and exposed to a magnetic treatment simulating a migratory flight to northern Egypt increased more in fuel load than control birds. By contrast, birds trapped during the late phase of the onset of autumn migration accumulated a high fuel load irrespective of magnetic treatment. Furthermore, early birds increased less in flight–muscle size than birds trapped later in autumn. We suggest that the relative importance of endogenous and environmental factors in individual birds is affected by the time of season and by geographical area. When approaching a barrier, environmental cues may act irrespective of the endogenous time programme.

“An eye for an eye?”—on the generality of the intimidating quality of eyespots in a butterfly and a hawkmoth

Large eyespots on the wings of butterflies and moths have been ascribed generally intimidating qualities by creating a frightening image of a bird or mammal much larger than the insect bearing the eyespots. However, evidence for this anti-predator adaptation has been largely anecdotal and only recently were peacock butterflies, Inachis io, shown to effectively thwart attacks from blue tits, Parus caeruleus. Here, we test whether large eyespots on lepidopterans are generally effective in preventing attacks from small passerines and whether the size of insect or bird can influence the outcome of interactions. We staged experiments between the larger eyed hawkmoths, Smerinthus ocellatus, and the smaller peacock butterflies, I. io, and the larger great tits, Parus major, and the smaller blue tits, P. caeruleus. Survival differed substantially between the insect species with 21 of 24 peacock butterflies, but only 6 of 27 eyed hawkmoths, surviving attacks from the birds. Thus, surprisingly, the smaller prey survived to a higher extent, suggesting that factors other than insect size may be important. However, great tits were less easily intimidated by the insects’ eyespots and deimatic behaviour and consumed 16 of 26, but the blue tits only 8 of 25, of the butterflies and hawkmoths. Our results demonstrate that eyespots per se do not guarantee survival and that these two insects bearing equally large eyespots are not equally well protected against predation.

Fixed eyespot display in a butterfly thwarts attacking birds

Eyespots have evolved in many lepidopteran insects, which suggests their adaptive value. One of their hypothesized functions is that predators are intimidated by prey with large and conspicuous eyespots and hence refrain from attacking them. Recent experiments have shown that a combination of eyespots and intimidating behaviour can increase survival. We tested whether the mere presence of conspicuous eyespots can thwart attacking birds, that is, when the eyespots are displayed constantly, without any intimidating behaviour. We used prey that consisted of wings of the peacock pansy butterfly, Junonia almana, glued onto a piece of cardboard so as to resemble a butterfly with its wings open. A mealworm was placed between the wings in place of the body. Great tits, Parus major, were used as the predator in the study and were offered a choice between two model prey, one with intact eyespots and one without. Prey with eyespots were attacked significantly fewer times than those without. The time between the first and second attack was longer when the prey without eyespots was attacked first. These results support the hypothesis that naturally occuring butterfly eyespots can increase survival even when they are constantly displayed and motionless.

Food intake and fuel deposition in a migratory bird is affected by multiple as well as single-step changes in the magnetic field.

SUMMARY Recent studies have shown that migratory thrush nightingales (Luscinia luscinia) experimentally treated with multiple changes of the magnetic field simulating a journey to their target stopover area in northern Egypt, increased fuel deposition as expected in preparation to cross the Sahara desert. To investigate the significance of food intake on the body mass changes observed, in the work described here we analysed food intake of the nightingales under study in those earlier experiments. Furthermore, to study whether a single change in the magnetic field directly to northern Egypt is sufficient to provide information for fuelling decisions, we performed a new experiment, exposing thrush nightingales trapped in Sweden, directly to a magnetic field of northern Egypt. Our results show that an experimentally induced magnetic field of northern Egypt, close to the barrier crossing, triggers the same response in fuel deposition as experiments with multiple changes of the magnetic field simulating a migratory journey from Sweden to Egypt, suggesting that migratory birds do not require successive changes in field parameters to incorporate magnetic information into their migratory program. Furthermore, irrespective of experimental set up (single or multiple changes of the magnetic field parameters) increase in food intake seems to be the major reason for the observed increase in fuelling rate compared with control birds, suggesting that geomagnetic information might trigger hormonal changes in migratory birds enabling appropriate fuelling behaviour during migration.

Winter predation on two species of hibernating butterflies: monitoring rodent attacks with infrared cameras

Documentation of predator attacks in nature is important for understanding how specific antipredator defences have evolved, but previous accounts have been mostly anecdotal. Therefore, we monitored predation on two closely related butterfly species, Aglais urticae and Inachis io, during winter hibernation. Butterflies were placed singly close to the floor on walls in dark, seminatural hibernation sites (e.g. unheated outhouses). We used motion-initiated infrared-sensitive cameras to record predator attacks on the butterflies. The antipredator attributes of the two species have two characteristics: during rest the butterflies reduce predators’ attention by mimicking leaves but they can suddenly change their guise by repeatedly flicking their wings. The wing flicking also produces hissing sounds and ultrasonic clicks and, furthermore, I. io, but not A. urticae, have large eyespots on the dorsal wing surface. The two butterfly species suffer from mouse predation during the winter and mice have been suggested as potential targets for the butterflies’ sound production. Results showed that (1) mice (Apodemus spp.) were important predators on butterflies, (2) I. io often survived attacks by wing-flicking behaviour, and (3) both species moved to less accessible positions after interactions with mice and other small mammalian predators, but I. io more often so. The successful predator evasion in darkness by I. io suggests a multimodal defence; in addition to the large eyespots, which intimidate birds, we suggest that the hissing and/or click sounds produced during wing flicking may have evolved as defence against rodent attacks.