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Antipredator defence in butterflies
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0001-7303-5632
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Predation exerts a potent selection mechanism and has resulted in a suite of antipredation adaptations encompassing morphological and behavioral traits in prey. In butterflies, several such traits appear to be directed towards birds which are considered as one of their major predators. In this thesis I have investigated tactics by which adult butterflies may survive close encounters with birds. In paper I, I provide supporting evidence that the small white “comma” on females of the comma butterfly, Polygonia c-album, has a distractive function on blue tits and so reduces the attack risk. In paper II & III, I investigate the antipredator efficiency of sudden wing-flicking in two species, the peacock butterfly, Inachis io, and the European swallowtail, Papilio machaon, when confronted with domestic fowl and great tits, respectively. Peacock butterflies were manipulated to either display visible or painted over eyespots. Interestingly, the birds that confronted peacocks with visible eyespots were more likely to utter antipredator alarm calls, which imply that the eyespots may be perceived as real eyes of a potential predator. On the whole, wing-flicking in both species typically induced evasion in the birds which suggests that the birds became frightened rather than perceiving the butterflies as not profitable to attack for some other reason. Moreover, I use blue tits as predators to investigate the possible function of smaller eyespots of satyrine butterflies in that they serve to divert predator attacks. Evidence suggests that low light conditions accentuated in the UV may enhance the deflective function of marginal eyespots in the woodland brown butterfly, Lopinga achine (paper IV). In paper V, I show that the presence of one marginal eyespot on the speckled wood butterfly, Pararge aegeria, can deflect bird attacks; moreover, when the butterfly is concealed against the background, eyespots can also increase the latency time until bird attack. In conclusion, my thesis underscores that behavioral studies of predators are instrumental to aid our understanding of the adaptive significance of certain behavioral and morphological traits in prey.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2013. , 25 p.
Keyword [en]
Antipredator defence, Bird, Crypsis, Predator, Predator-prey interaction, Prey-attack behavior, Butterfly, Deimatic behavior, Eyespots, Startle display
National Category
Ecology
Research subject
Animal Ecology
Identifiers
URN: urn:nbn:se:su:diva-88115ISBN: 978-91-7447-648-4 (print)OAI: oai:DiVA.org:su-88115DiVA: diva2:609643
Public defence
2013-04-26, Magnélisalen, Kemiska övningslaboratoriet, Svante Arrhenius väg 16 B, Stockholm, 10:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 1: Manuscript. Paper 5: Manuscript.

Available from: 2013-04-04 Created: 2013-03-06 Last updated: 2014-10-28Bibliographically approved
List of papers
1. The white “comma” as a distractive mark on the wings of comma butterflies – experimental tests in the lab and in the field: Distractive mark in a butterfly
Open this publication in new window or tab >>The white “comma” as a distractive mark on the wings of comma butterflies – experimental tests in the lab and in the field: Distractive mark in a butterfly
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Distractive marks have been suggested to prevent predator detection or recognition of a prey, by drawing the attention away from recognizable traits of the bearer. The white “comma” on the wings of comma butterflies (Polygonia c-album) has been suggested to represent such a distractive mark. In a laboratory experiment using blue tits as predators, we show that the comma on female butterflies effect their survival, since the blue tits attacked butterflies with over-painted commas more often than sham-painted butterflies with intact commas. There was no such effect with respect to male butterflies. Interestingly, the comma contrasts more against the uniformly brown ventral wing surface on females, than on the more variegated coloration of males. Hence, the comma can function as a distractive marking, at least when perceived against a uniformly coloured wing. In a field experiment we placed hibernating, similarly manipulated, comma butterflies on tree trunks of two different species and noted their survival. Although survival was higher on birch than on oak trees, there was no effect of our treatment, likely as a result of butterflies being preyed on by both diurnal and nocturnal predators, the latter of whom are unlikely to pay attention to distractive marks.

National Category
Ecology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-88114 (URN)
Funder
Swedish Research Council, 621-2007-5976
Available from: 2013-03-06 Created: 2013-03-06 Last updated: 2014-10-28Bibliographically approved
2. Eyespot display in the peacock butterfly triggers antipredator behaviors in naive adult fowl
Open this publication in new window or tab >>Eyespot display in the peacock butterfly triggers antipredator behaviors in naive adult fowl
Show others...
2013 (English)In: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 24, no 1, 305-310 p.Article in journal (Refereed) Published
Abstract [en]

Large conspicuous eyespots have evolved in multiple taxa and presumably function to thwart predator attacks. Traditionally, large eyespots were thought to discourage predator attacks because they mimicked eyes of the predators' own predators. However, this idea is controversial and the intimidating properties of eyespots have recently been suggested to Amply be a consequence of their conspicuousness. Some lepidopteran species include large eyespots in their antipredation repertoire. In the peacock butterfly, Mathis io, eyespots are typically hidden during rest and suddenly exposed by the butterfly when disturbed. Previous experiments have shown that small wild passerines are intimidated by this display. Here, we test whether eyespots also intimidate a considerably larger bird, domestic fowl, Gallus gallus domesticus, by staging interactions between birds and peacock butterflies that were sham-painted or had their eyespots painted oven Our results show that birds typically fled when peacock butterflies performed their display regardless of whether eyespots were visible or painted over. However, birds confronting butterflies with visible eyespots delayed their return to the butterfly, were more vigilant, and more likely to utter alarm calls associated with detection of ground-based predators, compared with birds confronting butterflies with eyespots painted over. Because production of alarm calls and increased vigilance are antipredation behaviors in the fowl, their reaction suggests that eyespots may elicit fear rather than just an aversion to conspicuous patterns. Our results, therefore, suggest that predators perceive large lepidopteran eyespots as belonging to the eyes of a potential predator.

Keyword
chicken, predator-prey interactions, startle display
National Category
Ecology Zoology Behavioral Sciences Biology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-87155 (URN)10.1093/beheco/ars167 (DOI)000312431000041 ()
Note

AuthorCount:5;

Available from: 2013-01-28 Created: 2013-01-28 Last updated: 2017-12-06Bibliographically approved
3. Deimatic Display in the European Swallowtail Butterfly as a Secondary Defence against Attacks from Great Tits
Open this publication in new window or tab >>Deimatic Display in the European Swallowtail Butterfly as a Secondary Defence against Attacks from Great Tits
2012 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 7, no 10, e47092- p.Article in journal (Refereed) Published
Abstract [en]

Background: Many animals reduce the risk of being attacked by a predator through crypsis, masquerade or, alternatively, by advertising unprofitability by means of aposematic signalling. Behavioural attributes in prey employed after discovery, however, signify the importance of also having an effective secondary defence if a predator uncovers, or is immune to, the prey's primary defence. In butterflies, as in most animals, secondary defence generally consists of escape flights. However, some butterfly species have evolved other means of secondary defence such as deimatic displays/startle displays. The European swallowtail, Papilio machaon, employs what appears to be a startle display by exposing its brightly coloured dorsal wing surface upon disturbance and, if the disturbance continues, by intermittently protracting and relaxing its wing muscles generating a jerky motion of the wings. This display appears directed towards predators but whether it is effective in intimidating predators so that they refrain from attacks has never been tested experimentally. Methodology/Principal Findings: In this study we staged encounters between a passerine predator, the great tit, Parus major, and live and dead swallowtail butterflies in a two-choice experiment. Results showed that the dead butterfly was virtually always attacked before the live butterfly, and that it took four times longer before a bird attacked the live butterfly. When the live butterfly was approached by a bird this generally elicited the butterfly's startle display, which usually caused the approaching bird to flee. We also performed a palatability test of the butterflies and results show that the great tits seemed to find them palatable. Conclusions/Significance: We conclude that the swallowtail's startle display of conspicuous coloration and jerky movements is an efficient secondary defence against small passerines. We also discuss under what conditions predator-prey systems are likely to aid the evolution of deimatic behaviours in harmless and palatable prey.

National Category
Ecology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-82967 (URN)10.1371/journal.pone.0047092 (DOI)000309831500136 ()
Note

AuthorCount:4;

Available from: 2012-12-13 Created: 2012-12-03 Last updated: 2017-12-06Bibliographically approved
4. Marginal eyespots on butterfly wings deflect bird attacks under low light intensities with UV wavelengths
Open this publication in new window or tab >>Marginal eyespots on butterfly wings deflect bird attacks under low light intensities with UV wavelengths
2010 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 5, no 5, e10798- p.Article in journal (Refereed) Published
Abstract [en]

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 day's 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.

National Category
Ecology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-45748 (URN)10.1371/journal.pone.0010798 (DOI)000278034600025 ()20520736 (PubMedID)
Funder
Swedish Research Council
Available from: 2010-11-10 Created: 2010-11-10 Last updated: 2017-12-12Bibliographically approved
5. Bird attacks on a butterfly with marginal eyespots and the role of prey concealment against the background: Marginal eyespots can deflect bird attacks
Open this publication in new window or tab >>Bird attacks on a butterfly with marginal eyespots and the role of prey concealment against the background: Marginal eyespots can deflect bird attacks
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Small eyespots on butterflies have long been thought to deflect attacks and birds are presumptive drivers selecting for these patterns. However, evidence of this function is still ambiguous. Marginal eyespots typically consist of a UV-reflective white pupil, surrounded by one black and one yellowish ring. We have recently shown that blue tits attack such eyespots, but only under low light intensities with accentuated UV-levels. An increased salience of the eyespots relative to the rest of the butterfly probably explains this result. Possibly, a background against which the butterfly is concealed may deceive birds to making similar errors. We therefore presented speckled wood butterflies provided with eyespots (or controls without eyespots) to blue tits against two backgrounds, oak- and birch bark. Results show that (i) eyespots, independent of background, were effective in deflecting attacks, (ii) the time elapsed between a bird’s landing and attack was interactively dependent on background and whether the butterfly bore an eyespot and (iii) the speed at which a butterfly was attacked predicted the outcome, with faster birds being more prone to errors than slower birds. This underscores a speed-accuracy tradeoff in the predators and that background plays a role in the defensive qualities of marginal eyespots.

National Category
Ecology
Research subject
Animal Ecology
Identifiers
urn:nbn:se:su:diva-88112 (URN)
Funder
Swedish Research Council, 621-2010-5579
Available from: 2013-03-06 Created: 2013-03-06 Last updated: 2014-10-28Bibliographically approved

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