Large Eyespots Research Articles

Wing morphology and eyespot pattern of Erebia medusa (Lepidoptera, Nymphalidae) vary along an elevation gradient in the Carpathian Mountains

Wing morphology and eyespot pattern of Erebia medusa (Lepidoptera, Nymphalidae) vary along an elevation gradient in the Carpathian Mountains

Buoys with looming eyes deter seaducks and could potentially reduce seabird bycatch in gillnets.

Bycatch of seabirds in gillnet fisheries is a global conservation issue with an estimated 400 000 seabirds killed each year. To date, no underwater deterrents trialled have consistently reduced seabird bycatch across operational fisheries. Using a combination of insights from land-based strategies, seabirds' diving behaviours and their cognitive abilities, we developed a floating device exploring the effect of large eyespots and looming movement to prevent vulnerable seabirds from diving into gillnets. Here, we tested whether this novel above-water device called ‘Looming eyes buoy' (LEB) would consistently deter vulnerable seaducks from a focal area. We counted the number of birds present in areas with and without LEBs in a controlled experimental setting. We show that long-tailed duck Clangula hyemalis abundance declined by approximately 20–30% within a 50 m radius of the LEB and that the presence of LEBs was the most important variable explaining this decline. We found no evidence for a memory effect on long-tailed ducks but found some habituation to the LEB within the time frame of the project (62 days). While further research is needed, our preliminary trials indicate that above-water visual devices could potentially contribute to reduce seabird bycatch if appropriately deployed in coordination with other management measures.

Do Hind Wing Eyespots of Caligo Butterflies Function in Both Mating Behavior and Antipredator Defense? (Lepidoptera, Nymphalidae)

Abstract In general, butterfly ventral hind wing eyespots are considered to play a role in predator–prey interactions. These eyespots are prominent wing pattern elements in Brassolini butterflies, and they vary in size, position, and number across taxa. Female Caligo Hübner, 1819 (Lepidoptera, Nymphalidae) appear to use the large eyespots of lekking males as a mate-locating cue, but female Opsiphanes Doubleday, 1849 (Lepidoptera, Nymphalidae) do not because males patrol to find mates. These behaviors led us to predict that male Caligo should have larger eyespots than females, but eyespot size would not differ between sexes in Opsiphanes. Our analyses supported these predictions. As displacement of the eyespots to the center of the wing might make them more conspicuous, we asked if eyespot position and size covaried across the Brassolini phylogeny. While we found a positive association between position and size, the relationship of these two variables contained significant phylogenetic signal. Two Brassolini species show strong sexual dimorphism where females converge on the color pattern of sympatric species of Caligo. Their ventral hind wing eyespots are much larger than those of close relatives, approximating those of Caligo, and further reinforcing the importance of ventral hind wing eyespots as a visual signal in this group of butterflies. Importantly, our results suggest that, in addition to antipredation defense, ventral hind wing eyespots can function in mating activities, and consequently they might be evolving under both natural and sexual selection in Caligo butterflies.

Lizards as Predators of Butterflies: Shape of Wing Damage and Effects of Eyespots

In warm climates, lizards may be important as predators of butterflies and thus exert selection pressure on butterfly colour patterns, including eyespots. However, this has received little attention. Two studies reported no evidence that butterfly eyespots deflect lizard attacks, while possible intimidating effects of butterfly eyespots on lizards have not been investigated. We exposed common evening brown butterflies (Melanitis leda) with a wide range of eyespot sizes (dry season forms with very small and faint eyespots, intermediate phenotypes with small eyespots, and wet season forms with large or very large eyespots) to house geckos, and recorded the location and shape of wing surface loss. We supplemented these data with direct observations of attacks of house geckos (Hemidactylus frenatus) and bronze skinks (Eutropis macularia) on common evening brown butterflies. We found that about three quarters of symmetrical wing surface loss, and about half of the non-symmetrical wing surface loss was rounded like the mouth of a gecko. Symmetrical as well as non-symmetrical wing surface loss was significantly more common in hindwings. We surmise that rounded wing surface loss and a bias in symmetrical wing surface loss to hindwings can be taken as evidence for failed lizard attacks. Rounded wing surface loss was more common in butterflies with small eyespots than in those with very small eyespots or with large eyespots. This suggests that small eyespots can deflect lizard attacks away from the head towards the wing margins, and that large eyespots can thwart lizard attacks. In four cases, skinks appeared to explore rather than attack butterfly eyespots. In contrast to earlier studies, our data provide evidence that butterfly eyespots can be an effective defence against lizards, and thus that predation by lizards can select for eyespots in butterflies.

Natural History ofSelenophanes cassiope guarany(Lepidoptera: Nymphalidae: Brassolini): an Integrative Approach, From Molecules to Ecology

Brassolines are among the largest Neotropical butterflies, with large eyespots resembling vertebrate eyes in their wings. Some subspecies of co-occurring brassolines show striking similarities in wing traits to the extent that mimicry within the tribe has been suggested. When adults exhibit phenotypic convergence, data on immature stages can be used to uncover similarities derived from common descent. Here, evidence for future phylogenies to support Selenophanes relatedness to either Opsiphanes or Catoblepia are provided by comparing novel molecular (barcode sequence) and morphological (immature) data. While barcoding showed Selenophanes sequences to be nested within Catoblepia, with intergeneric distances smaller than between Catoblepia species, the state of the art of immature morphological descriptions showed that Catoblepia and Opsiphanes were more similar than either were to Selenophanes. Despite their popularity, brassolines are difficult to find in nature, partly because they are active during dawn and dusk. S. cassiope is a rare species, so the hitherto unknown female of S. cassiope guaranyCasagrande, 1992 is described, as well as morphologically and ecologically relevant adult traits. Analysis of sensory organs revealed a possible reversal of brassoline adaptations to the crepuscular habit. The pigment class of wing cells from several regions with different colors was melanin, except for white (colorless) scales. Multitrophic interactions with an Arecaceae host plant, and egg (Anastatus sp., Galeopsomyia sp.) and pupal (Eurytoma sp.) parasitoids are also reported. This integrative approach benefits from a group with great potential to explore the interplay, from molecules to ecology, of adaptive evolution.

Attack risk for butterflies changes with eyespot number and size.

Butterfly eyespots are known to function in predator deflection and predator intimidation, but it is still unclear what factors cause eyespots to serve one function over the other. Both functions have been demonstrated in different species that varied in eyespot size, eyespot number and wing size, leaving the contribution of each of these factors to butterfly survival unclear. Here, we study how each of these factors contributes to eyespot function by using paper butterfly models, where each factor is varied in turn, and exposing these models to predation in the field. We find that the presence of multiple, small eyespots results in high predation, whereas single large eyespots (larger than 6 mm in diameter) results in low predation. These data indicate that single large eyespots intimidate predators, whereas multiple small eyespots produce a conspicuous, but non-intimidating signal to predators. We propose that eyespots may gain an intimidation function by increasing in size. Our measurements of eyespot size in 255 nymphalid butterfly species show that large eyespots are relatively rare and occur predominantly on ventral wing surfaces. By mapping eyespot size on the phylogeny of the family Nymphalidae, we show that these large eyespots, with a potential intimidation function, are dispersed throughout multiple nymphalid lineages, indicating that phylogeny is not a strong predictor of eyespot size.

On the deterring effect of a butterfly’s eyespot in juvenile and sub-adult chickens

Abstract Circular patterns, or eyespots, are common anti-predator features in a variety of animals. Two defensive functions have been documented: large eyespots may intimidate predators, whereas smaller marginal eyespots may divert attacks. However, a given eyespot potentially serves both functions, possibly depending on the predator’s size and/or experience. Naïve predators are potentially more likely to misdirect their attacks towards eyespots; alternatively, their typically smaller size would make them more intimidated by the same eyespots. Here we test how juvenile and sub-adult naïve chickens respond to a single eyespot on a butterfly’s wing. We presented the birds with dead wall brown butterflies, Lasiommata megera, that had their apical eyespot visible or painted over. We assessed the birds’ responses’ by (i) scoring their intimidation reaction, (ii) whether they uttered alarm calls and, (iii) if they attacked the butterfly and where they targeted their attacks. Results show that both age categories received higher intimidation scores when offered a butterfly with a visible eyespot. Juveniles were more intimidated by the butterfly than the sub-adults: they received higher intimidation scores and were more prone to utter alarm calls. Moreover, only sub-adults attacked and did so by preferentially attacking the butterfly’s anterior. We demonstrate an intimidating effect of the type of eyespot that has previously been shown only to divert attacks. We suggest that one and the same eyespot may serve two functions relative to different predators; however, further experiments are needed to disentangle the role of predator identity and its link to size, ontogeny and experience.

Body size affects the evolution of eyespots in caterpillars

Many caterpillars have conspicuous eye-like markings, called eyespots. Despite recent work demonstrating the efficacy of eyespots in deterring predator attack, a fundamental question remains: Given their protective benefits, why have eyespots not evolved in more caterpillars? Using a phylogenetically controlled analysis of hawkmoth caterpillars, we show that eyespots are associated with large body size. This relationship could arise because (i) large prey are innately conspicuous; (ii) large prey are more profitable, and thus face stronger selection to evolve such defenses; and/or (iii) eyespots are more effective on large-bodied prey. To evaluate these hypotheses, we exposed small and large caterpillar models with and without eyespots in a 2 × 2 factorial design to avian predators in the field. Overall, eyespots increased prey mortality, but the effect was particularly marked in small prey, and eyespots decreased mortality of large prey in some microhabitats. We then exposed artificial prey to naïve domestic chicks in a laboratory setting following a 2 × 3 design (small or large size × no, small, or large eyespots). Predators attacked small prey with eyespots more quickly, but were more wary of large caterpillars with large eyespots than those without eyespots or with small eyespots. Taken together, these data suggest that eyespots are effective deterrents only when both prey and eyespots are large, and that innate aversion toward eyespots is conditional. We conclude that the distribution of eyespots in nature likely results from selection against eyespots in small caterpillars and selection for eyespots in large caterpillars (at least in some microhabitats).

Temporal Gene Expression Variation Associated with Eyespot Size Plasticity in Bicyclus anynana

Seasonal polyphenism demonstrates an organism's ability to respond to predictable environmental variation with alternative phenotypes, each presumably better suited to its respective environment. However, the molecular mechanisms linking environmental variation to alternative phenotypes via shifts in development remain relatively unknown. Here we investigate temporal gene expression variation in the seasonally polyphenic butterfly Bicyclus anynana. This species shows drastic changes in eyespot size depending on the temperature experienced during larval development. The wet season form (larvae reared over 24°C) has large ventral wing eyespots while the dry season form (larvae reared under 19°C) has much smaller eyespots. We compared the expression of three proteins, Notch, Engrailed, and Distal-less, in the future eyespot centers of the two forms to determine if eyespot size variation is associated with heterochronic shifts in the onset of their expression. For two of these proteins, Notch and Engrailed, expression in eyespot centers occurred earlier in dry season than in wet season larvae, while Distal-less showed no temporal difference between the two forms. These results suggest that differences between dry and wet season adult wings could be due to a delay in the onset of expression of these eyespot-associated genes. Early in eyespot development, Notch and Engrailed may be functioning as repressors rather than activators of the eyespot gene network. Alternatively, temporal variation in the onset of early expressed genes between forms may have no functional consequences to eyespot size regulation and may indicate the presence of an 'hourglass' model of development in butterfly eyespots.

Eyespot display in the peacock butterfly triggers antipredator behaviors in naïve adult fowl

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 simply be a consequence of their conspicuousness. Some lepidopteran species include large eyespots in their antipredation repertoire. In the peacock butterfly, Inachis 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 over. 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.

Polyphemus Moth Antheraea polyphemus (Cramer) (Insecta: Lepidoptera: Saturniidae: Saturniinae)

The polyphemus moth, Antheraea polyphemus (Cramer), is one of our largest and most beautiful silk moths. It is named after Polyphemus, the giant cyclops from Greek mythology who had a single large, round eye in the middle of his forehead. The name is because of the large eyespots in the middle of the moth’s hind wings. This 9-page fact sheet was written by Donald W. Hall and published by the UF Department of Entomology and Nematology, August 2012. EENY-531/IN945: Polyphemus Moth Antheraea polyphemus (Cramer) (Insecta: Lepidoptera: Saturniidae: Saturniinae) (ufl.edu)

Structural analysis of eyespots: dynamics of morphogenic signals that govern elemental positions in butterfly wings.

BackgroundTo explain eyespot colour-pattern determination in butterfly wings, the induction model has been discussed based on colour-pattern analyses of various butterfly eyespots. However, a detailed structural analysis of eyespots that can serve as a foundation for future studies is still lacking. In this study, fundamental structural rules related to butterfly eyespots are proposed, and the induction model is elaborated in terms of the possible dynamics of morphogenic signals involved in the development of eyespots and parafocal elements (PFEs) based on colour-pattern analysis of the nymphalid butterfly Junonia almana.ResultsIn a well-developed eyespot, the inner black core ring is much wider than the outer black ring; this is termed the inside-wide rule. It appears that signals are wider near the focus of the eyespot and become narrower as they expand. Although fundamental signal dynamics are likely to be based on a reaction-diffusion mechanism, they were described well mathematically as a type of simple uniformly decelerated motion in which signals associated with the outer and inner black rings of eyespots and PFEs are released at different time points, durations, intervals, and initial velocities into a two-dimensional field of fundamentally uniform or graded resistance; this produces eyespots and PFEs that are diverse in size and structure. The inside-wide rule, eyespot distortion, structural differences between small and large eyespots, and structural changes in eyespots and PFEs in response to physiological treatments were explained well using mathematical simulations. Natural colour patterns and previous experimental findings that are not easily explained by the conventional gradient model were also explained reasonably well by the formal mathematical simulations performed in this study.ConclusionsIn a mode free from speculative molecular interactions, the present study clarifies fundamental structural rules related to butterfly eyespots, delineates a theoretical basis for the induction model, and proposes a mathematically simple mode of long-range signalling that may reflect developmental mechanisms associated with butterfly eyespots.

Auditory defence in the peacock butterfly (Inachis io) against mice (Apodemus flavicollis and A. sylvaticus)

Morphological and behavioural traits can serve as anti-predator defence either by reducing detection or recognition risks, or by thwarting initiated attacks. The latter defence is secondary and often involves a ‘startle display’ comprising a sudden release of signals targeting more than one sensory modality. A suggested candidate for employing a multimodal defence is the peacock butterfly, Inachis io, which, by wing-flicking suddenly, produces sonic and ultrasonic sounds and displays four large eyespots when attacked. The eyespots make small birds retreat, but whether the sounds produced thwart predator attacks is largely unknown. Peacocks hibernate as adults in dark wintering sites and employ their secondary defence upon encounter with small rodent predators during this period. In this study, we staged predator–prey encounters in complete darkness in the laboratory between wild mice, Apodemus flavicollis and Apodemus sylvaticus, and peacocks which had their sound production intact or disabled. Results show that mice were more likely to flee from sound-producing butterflies than from butterflies which had their sound production disabled. Our study presents experimental evidence that the peacock butterfly truly employs a multimodal defence with different traits targeting different predator groups; the eyespots target birds and the sound production targets small rodent predators.

Number of eyespots and their intimidating effect on naïve predators in the peacock butterfly

Predation experiments have shown that the large eyespots (concentric rings of contrasting colors) found on the wings of several lepidopteran species intimidate passerine predators. According to the eye mimicry hypotheses, the intimidation is caused by predators associating the eyespots with the presence (of the eyes) of their own enemy. The conspicuousness hypothesis suggests, instead, that it is simply the conspicuousness of eyespot patterns that is intimidating, possibly due to a sensory bias. We studied how the number of eyespots, 2 or 4, influences intimidation. We predicted that if eye mimicry is important, the maximum response would be reached with a pair of eyespots. On the other hand, if conspicuousness is important, then more than 2 eyespots should result in an even stronger response. The peacock butterfly, Inachis io, has 4 large eyespots on its wings. We presented naïve insectivorous birds (pied flycatcher, Ficedula hypoleuca) 2 different prey items made from wings of dead peacock butterflies and a mealworm between the wings. One group of birds received prey that had no or only 2 eyespots visible and the other group received prey that had no or all 4 eyespots visible. Eyespots clearly increased hesitation before attacks. Because the birds were naïve, this difference in response to the eyespots was innate. Importantly, there was no difference in attack latency between 2 and 4 eyespots. We conclude that it is unlikely that conspicuousness as such has selected for eyespots in the peacock butterfly.

Deflective effect and the effect of prey detectability on anti-predator function of eyespots

Eyespots (patterns of roughly concentric rings) are often thought to have an anti-predator function. Previous experiments have lent support for the intimidation hypothesis by demonstrating a deterring effect of eyespots, but so far there is little evidence for the deflective effect (direction of attacks toward less vital body parts). We studied predators’ responses towards large and small eyespots and towards prey with no, one, or a pair of eyespots and if this response is influenced by whether or not prey blend into background. In two experiments, we used artificial, triangular prey items and blue tits (Cyanistes caeruleus) as predators. In experiment 1, we found evidence for the deflective effect of small but not large eyespots, independent of whether the prey was presented on a concealing or exposing background. In experiment 2, we found that predators avoided the prey with a pair of small eyespots more than the prey without eyespots, but interestingly, we only found this deterring effect on the concealing background. There was no difference in attacks between the prey with one large and two small or one large and no eyespots. We conclude that deflective function may select for eyespots, and background may influence the deterring function of eyespots.

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.

Four new species of fan worms (Polychaeta: Sabellidae) from worldwide localities

Four new species of soft-bottom sabellid polychaetes are described and illustrated. Branchiomma costaricensis n. sp. is described from 31 m depth off Isla del Coco, Costa Rica; Dialychone arabica n. sp. from 105 m depth in the Arabian Sea; Dialychone blakei n. sp. from 487 m depth off Louisiana in the Gulf of Mexico and Paradialychone harrisae n. sp. from 30 m depth in southern California. Branchiomma costaricensis n. sp. is characterized by having microstylodes with the median pair 1.5 times longer than neighbouring pairs, thoracic uncini with two rows of teeth above the main fang, an unspotted body and large interramal eyespots. Dialychone arabica n. sp. has the anterior peristomial ring lobe exposed beyond the collar and a pre-pygidial depression occupying eight segments. In D. blakei n. sp., the anterior peristomial ring lobe is not exposed beyond the collar, the pre-pygidial depression occupies the last four segments and the posterior segments possess thin elongate, narrowly hooded chaetae. Paradialychone harrisae n. sp. differs from the other species of the genus in having the anterior peristomial ring lobe bilobed and exposed beyond the collar, a rectangular ventral collar shield and paleate chaetae with a long mucro.

“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.

Crypsis versus intimidation—anti-predation defence in three closely related butterflies

Butterflies that hibernate exhibit particularly efficient defence against predation. A first line of defence is crypsis, and most hibernating butterflies are leaf mimics. When discovered, some species have a second line of defence; the peacock, I. io, when attacked by a predator flicks its wings open exposing large eyespots and performs an intimidating threat display. Here we test the hypothesis that butterflies relying solely on leaf mimicking and butterflies with an intimidating wing pattern, when attacked, exhibit different behavioural suites—because leaf mimicking is best implemented by immobility, whereas intimidating coloration is best implemented by intimidating behaviour. In laboratory experiments blue tits, Parus caeruleus, were allowed 40 min to attack single individuals of three species of butterfly: one relying solely on crypsis, the comma, Polygonia c-album; one relying on intimidating wing pattern in addition to crypsis, the peacock; and one intermediate species, the small tortoiseshell Aglais urticae. The results are in accordance with expectations and demonstrate that: (1) birds take longer to discover the leaf mimicking species, the comma, than the tortoiseshell and the peacock; (2) the comma remained motionless throughout experimental trials but small tortoiseshells and peacocks flicked their wings when attacked; (3) the most intimidating butterfly, the peacock, started flicking its wings at a greater distance from the attacking bird than the small tortoiseshell; and (4) the intimidating pattern and behaviour of peacocks was effective—when discovered, all peacocks survived interactions with blue tits, whereas only 22% of commas and 8% of small tortoiseshells survived.

Artificial selection on the shape of reaction norms for eyespot size in the butterfly Bicyclus anynana: direct and correlated responses

Abstract The tropical butterfly Bicyclus anynana shows phenotypic plasticity in its ventral wing pattern as an adaptive response to wet-dry seasonality. Wet season form individuals have large eyespots, whereas individuals of the dry season generation have small eyespots. In the laboratory these forms can be obtained by rearing larvae at high and low temperatures, respectively. To study the extent to which the shape of the nearly linear reaction norms for eyespot size can be changed we applied four generations of sib selection by rearing full-sib families across three temperatures. In addition, we measured ecdysteroid titres shortly after pupation in the final generation. Although phenotypic variation in shape was present initially, the experiment yielded lines with reaction norms with similar shapes but different elevations. High, positive genetic correlation across temperatures can explain this lack of response. Differences in ecdysteroid titres did not readily relate to differences in eyespot size.