© Entomologica Fennica. 22 October 2001 Convergence in wing coloration between orange underwing moths (Archiearis spp.) and tortoiseshell butterflies (Aglais spp.) Jens Rydell, Joakim Fagerström, Staffan Andersson, Gabriela Gamberale Stille, Magnus Gelang, Winston C. Lancaster, Mats G. E. Svensson & Brigitta S. Tullberg Rydell, J., Fagerström, J., Andersson, S., Stille, G. G., Gelang, M., Lancaster, W. C., Svensson, M. G. E. & Tullberg, B. S. 2001: Convergence in wing coloration between orange underwing moths (Archiearis spp.) and tortoise- shell butterflies (Aglais spp.). — Entomol. Fennica 12: 65–71. We analysed the wing coloration of the orange underwing moth Archiearis parthenias (Geometridae, Archiearinae) in comparison with the small tor- toiseshell butterfly Aglais urticae (Nymphalidae). Both species fly in early spring and occur sympatrically in the northern Palaearctic. Aglais, the more common species, has a longer flight period and uses a broader range of habitats. Both species show a camouflaged colour pattern on surfaces exposed at rest but a bright orange signal in flight. Although the evolution of its coloration is constrained by its geometrid morphology, Archiearis is function- ally similar to Aglais both while resting and in flight. Archiearis has presum- ably evolved from nocturnal geometrid ancestors. Its shift to diurnality has included a change in the predator defence system from one based on ultrasonic hearing, functional against bats, to one presumably functional against birds. Preliminary palatability tests showed that Aglais is distasteful to birds (chicken), while Archiearis seems to be palatable. The function of the convergent coloration is unknown, but several possibilities are discussed. Jens Rydell, J. Fagerström, S. Andersson, M. Gelang & W. C. Lancaster, Zoology Department, Göteborg University, P.O. Box 463, SE-405 30 Göteborg, Sweden G. Gamberale Stille & B. S. Tullberg, Zoology Department, Stockholm University, SE-106 91 Stockholm, Sweden M. G. E. Svensson, Department of Chemical Engineering, Lund University, P.O. Box 118, SE-221 00 Lund, Sweden W. C. Lancaster, School of Osteopathic Medicine, Pikeville College, Pikeville KY 41501, U.S.A. Received 13 October 2000, accepted 15 May 2001 1. Introduction defences against birds include visual concealment or crypsis (Cott 1940, Kettlewell 1955, 1959, An adequate predator defence system is essential Edmunds 1990), aposematic or mimetic signals for the survival of any animal population. Insect (Bates 1862, Poulton 1890, Cott 1940, Wickler 66 Rydell et al. • ENTOMOL. FENNICA Vol. 12 1968, Rettenmeyer 1970, Benson 1972, Roths- infans are bright orange and black (Skou 1984, child 1985, Waldbauer 1988, Guilford 1990) and Covell 1984). This coloration is otherwise rare probably startle signals (Sargent 1990). Crypsis among holarctic geometrids but shows limited and aposematism or mimicry are often comple- similarity to those of some common, sympatric mentary, frequently occurring on the same ani- nymphalid butterflies including e.g. the tortoise- mal although usually on different parts of it (“in- shell Aglais urticae of the Palaearctic (Stoltze tegrated defence systems”; Edmunds 1974). For 1996) and Milbert’s tortoiseshell Nymphalis example, many Lepidoptera such as the small tor- milberti of the Nearctic (Scott 1986). We suggest toiseshell butterfly Aglais urticae (L.) are cam- that through the shift to diurnality (Surlykke et ouflaged when the wings are folded but show al. 1997) and range expansion to the northern bright coloration when alert and in flight. Further- Holarctic, the archiearines have adopted a colora- more, the same colour pattern may serve two or tion that functionally resembles the tortoiseshell more functions depending on the situation (“dual butterflies and some other similarly coloured signals”; Rothschild 1975, Brown 1988). For ex- nymphalid butterflies. ample, a signal may be aposematic or mimetic at close range but cryptic at a distance (Papageorgis 1975, Endler 1978, 1981). 2. Wing colour and its distribution The Archiearinae is a small (12 species) and exclusively diurnal subfamily among the Geo- The dorsal and ventral surfaces of ten dried and metridae, which otherwise consists mostly of noc- spread individuals of each of the two species, turnal moths (Scoble 1992). The subfamily is be- obtained from the Natural History Museum in lieved to have originated in the southern hemi- Göteborg, were photographed against a white sphere (McQuillan in Common 1990), and the background, and the pictures were then scanned present distribution includes the mountains of (resolution 150 DPI) using Hewlett-Packard Tasmania, Patagonia, North America and the ScanJet 6100C and edited using Adobe Photo- northern Palaearctic including Japan. Character- shop. Only the right wing pair of each specimen istically, the Archiearinae have camouflaged (all males) was analysed. Forewings and hind- forewings but hindwings show a high-contrast pat- wings were treated separately. For each wing, we tern in black and either white, yellow or orange determined the total area (in cm2) and for the up- (Prout 1932, Common 1990, E. Schmidt-Nielsen per and lower wing surfaces also the area covered pers. comm.). The hindwing colours of the two by (a) black and dark grey colours, (b) brown, northern Palaearctic species Archiearis parthenias (c) white and yellow and (d) orange. and A. notha as well as that of the Nearctic A. On five specimens of each species, we meas- Table 1. Total wing areas (cm2) and the area of each of four colour categories on dorsal and ventral sides of the right wings of Archiearis parthenias and Aglais urticae (n = 10 for each species). “Total” implies the sum of the areas of the dorsal and ventral wing surfaces. ————————————————————————————————————————————————— A. parthenias A. urticae —————————— —————————— mean S.D. mean S.D. t p ————————————————————————————————————————————————— Total area 3.65 0.33 9.06 0.57 8.25 <0.001 Black, total 0.50 0.10 3.69 0.28 10.77 <0.001 Brown, total 1.90 0.25 3.59 0.33 4.09 <0.001 White/yellow, total 0.15 0.04 0.71 0.06 8.16 <0.001 Orange, total 1.11 0.11 1.12 0.13 0.06 n.s. dorsal forewing 0.00 – 0.68 0.09 7.75 <0.001 dorsal hindwing 0.33 0.05 0.44 0.07 1.30 n.s. ventral forewing 0.49 0.06 0.00 – 8.50 <0.001 ventral hindwing 0.29 0.04 0.00 – 6.62 <0.001 ————————————————————————————————————————————————— ENTOMOL. FENNICA Vol.12 • Wing coloration in Archearis 67 Fig. 1. Average spectral reflectance (mean + S.D.) of the orange wing col- oration in Archiearis par- thenias (solid line; n = 5) and Aglais urticae (dashed line; n = 5). To illustrate the close resemblance in spectral shape (i.e. colour), spectra were set to the same overall brightness (total reflectance 300– 700 nm). ured the reflected radiance from the orange parts the upper side. of the wings, using a PS 1000 UV/VIS diode-ar- To the human eye, the orange colour of ray spectrometry equipment (Ocean Optics Inc., Archiearis appears very similar to that of Aglais. Dunedin, USA) described by Andersson (1996). The reflectance curves, controlled for brightness, The reflectance probe, consisting of one reading show that spectral shape (colour) is very similar fiber surrounded by six illuminating fibers, was across the entire 300–700 nm spectral range mounted perpendicularly to the wing surface and (Fig. 1). Archiearis was somewhat brighter than at a distance giving a measuring spot approxi- Aglais (14 units in CIE L*, corresponding to about mately 1.5 mm in diameter. Reflectance was cal- one step on a 10-step grey scale), but brightness culated in relation to a SpectralonTM white stand- is of little importance in prey recognition com- ard. The average of three scans from each speci- pared to colour variables. Coefficients in the men was used. To facilitate comparisons of col- CIELAB colour space (computed on the original our properties (spectral shape), the average spectra) were also similar. Hue angle (h ) differed ab reflectance spectra from the two species were set by only 0.8 degrees (there is a 90 degree differ- to the same brightness (R ). We also com- ence between a pure red and pure yellow) and 300–700 puted coefficients for hue (h ) and chroma (C ) chroma by 4.4 units (on a 0–100 scale; Aglais ab ab in the human CIELAB colour space (D65 day- being slightly more chromatic). Both these dif- light, 10-degree observer; C.I.E. 1971). ferences are below the least detectable differences Both Archiearis parthenias and Aglais urticae to the human eye (Wyszecki & Stiles 1982), and show a mixture of camouflage (black, brown and most likely to birds as well. white/yellow) and bright orange. The camouflage pattern of Archiearis is on the dorsal side of the forewings in a typical geometrid manner, while 3. Palatability tests the camouflage of Aglais is on the entire ventral surface of the wings, typical of butterflies, in both Archiearis and Aglais used for palatability tests cases covering the wing surfaces exposed at rest. were caught in daytime by hand netting in birch Although Archiearis is less than half the size of woodlands near Göteborg, southern Sweden Aglais, the total area of orange on the wings is the (57°N) in April 1997 and 1998 or near Stockholm same for both species (Table 1). In Archiearis, (60°N) in April 1997. They were kept alive in a the orange “signal” colour is on the upper side of refrigerator at 6 °C until the experiment, which the hindwings and on the ventral side of both took place at most 5 days after capture. Two to wings, while in Aglais the orange is entirely on four week old domestic chicks, which had no pre- 68 Rydell et al. • ENTOMOL. FENNICA Vol. 12 vious experience with Lepidoptera, were used as and Archiearis, 0/4) suggests that Aglais may be predators. They arrived from the hatchery when more distasteful than Archiearis. However, the < 20 hours old, were fed with chick starter crumbs sample size was small and the difference not quite and live mealworms and housed in a 100 ¥ 55 ¥ significant (Fisher’s Exact Test; p = 0.088). 20-cm cage and heated with a 60-W carbon light bulb. The cage had wooden sides, steel-net floor made partly of wood and chicken wire and a floor 4. Discussion covered with sawdust. The palatability tests took place in the same Archiearis parthenias, its congener A. notha and kind of cage, covered with a fine net and partly Aglais urticae occur sympatrically over much of screened off, leaving a 30 ¥ 55-cm testing arena. the northern Palaearctic (Skou 1984, Stoltze The insects, which were released in the testing 1996). Both Aglais and Archiearis are active only cage one at a time, could be reached everywhere during the day and fly in sunshine. In southern in the cage. As controls, we used the speckled Scandinavia, Archiearis usually emerges in April. wood butterfly Pararge aegeria (Satyrinae), Adult Aglais urticae emerge in August, fly which is palatable to birds (Tullberg & Gamberale throughout the autumn, overwinter and then fly Stille unpubl.), and these were given to each chick again from March to May (Svensson 1993). before and after the test insects. Thirteen chicks Archiearis parthenias lives in birch forest and A. were presented with four Aglais and four chicks notha on aspen (Skou 1984), but Aglais urticae were presented with two Archiearis each. uses a much broader range of habitats than the The chicks usually started to hunt the control archiearines (Thomas & Lewington 1991, Stoltze butterfly (Pararge aegeria) a few seconds after it 1996). Hence, the distribution and flight period was released in the test cage. In two cases it failed of the butterfly encompass those of the Ar- to catch the butterfly, but all that were caught were chiearines. eaten. Each chick attacked at least one Aglais The orange underwing moths (Archiearinae) urticae, but several did not attack more than one. presumably evolved from a nocturnal geometrid The proportion that were attacked differed sig- ancestor but are entirely diurnal. They are nificantly between Pararge aegeria (the control; equipped with tympanic organs, which in other mean 0.94) and Aglais urticae (the test insects; geometrids are used for defence against echo- mean 0.67) (Wilcoxon’s Matched Pairs test: locating bats (Surlykke & Filskov 1997), but that n = 13, Z = 2.55, p = 0.011), indicating that Aglais no longer function for this purpose (Surlykke et was sometimes avoided upon sight. Seven of the al. 1997). At the same time, they have evolved 13 chicks left all Aglais uneaten whereas six con- wing coloration that differs drastically from that sumed at least one. The proportion eaten was of most other geometrids but closely resembles significantly higher for Pararge (mean 1.0) than that of sympatric and distasteful butterflies. for Aglais (mean 0.39) (Wilcoxon’s Matched Pairs Archiearis and Aglais are very different in test: n = 13, Z = 2.80, p = 0.005). Thus, Aglais appearance with outspread wings. This relates to urticae was unpalatable compared to the control. differences in size and in the distribution of col- All of the four chicks that were presented with our on the wings. In the field, however, the two Archiearis parthenias and ate Pararge aegeria, insects show very similar signals. The orange parts also attacked both moths. There was thus no indi- of the wings are virtually identical in coloration cation that they were avoided upon sight. Moreo- and size and are displayed only in flight. At rest, ver, three of the chicks ate both Archiearis indi- butterflies and moths fold their wings differently, viduals and one chick ate one but not the other. and the distribution of camouflaged coloration The proportion eaten of those that were attacked reflects the portions of the wings that are visible. does not differ significantly between Pararge and That the camouflaged parts are different in size Archiearis (Paired t-test: t = 1.00, d.f. = 3, and location on the wings may be irrelevant, since p = 0.39), but this could be due to small sample camouflage is a “non-signal” (Wickler 1968). size. A comparison of the proportion of chicks Hence the apparent difference in coloration be- that did not eat any of the test insects (Aglais, 7/13 tween Archiearis and Aglais may be illusory. ENTOMOL. FENNICA Vol.12 • Wing coloration in Archearis 69 Because of morphological constraints imposed by Although these explanations cannot be excluded its ancestry, Archiearis have adopted a novel dis- with the data at hand, they seem unlikely in our tribution of colour patterns and achieved a func- case. They do not explain the observed conver- tional similarity in appearence to Aglais both in gence in the signal of Archiearis towards that of flight and at rest. Aglais. What is the function of the orange signal Although the colour vision of birds differs shown in flight? Earlier work has indicated that from that of humans in several respects, such as Aglais is distasteful to birds (Pocock 1911, Blest UV vision and tetrachromacy (Varela et al. 1993), 1957) and mammals (Møhl & Miller 1976), and we believe that it is a reasonable assumption that our results support this conclusion. Our limited birds cannot tell apart the Archiearis and Aglais experiment did not provide any evidence that wing colours. Firstly, the UV waveband contained Archiearis is distasteful to birds (chicks in the no additional difference in reflectance shape (col- present study). Hence, it seems possible that a our). Secondly, the subtle difference is located in flying Archiearis could be a Batesian mimic of a the orange-red spectral region, where human col- flying Aglais, which probably is aposematic. To our resolution peaks and outperforms other known test this hypothesis conclusively, it would be nec- visual systems (Neumeyer 1991), including re- essary to investigate whether predators (birds) cent models of avian colour space (Vorobyev et generalize between flying Archiearis and Aglais. al. 1998). The barely perceivable difference in The presence of both camouflage and bright terms of human CIE coefficients strongly suggests wing surfaces in Aglais and Archiearis (and in that the two orange colours are indistinguishable many other butterflies and moths) suggests that for birds. the situation is often more complex than this and Even if the colour convergence seems con- that movement is also involved in the insect’s sig- vincing, however, predators might distinguish nalling strategy. Many predators detect prey by prey based on other visual cues. For example, the movement, and animals therefore increase the risk rufous-tailed jacamar Galbula ruficauda, a neo- of being detected when they move. At the same tropical butterfly specialist, recognizes palatable time they become more difficult to catch. There- mimics of Heliconius spp. and other butterflies fore, many animals including Aglais and Ar- by subtle differences in flight characteristics (Chai chiearis forego crypsis as a defence when they & Srygley 1990). Likewise, Müllerian mimics take flight (Wiklund & Sillén-Tullberg 1985) and among Lygaeus bugs must be almost identical to shift to a bright signal. The fact that Aglais shifts achieve full mutual protection from predation by from camouflage to orange signalling when it is great tits Parus major (Wiklund & Järvi 1982). ready to move suggests that its distastefulness is On the other hand, a predator may have little not strong enough to provide efficient protection chance to notice details of a prey that is moving from predation, unless it is also alert and able to rapidly and erratically, as in the case of Archiearis, move rapidly and erratically. A flying Aglais is particularly if the predator is a non-specialist like presumably difficult to catch; therefore its ex- a migratory bird. Hence, according to Fisher pected value for a predator is lower than that of a (1958), “conspicuously different insects may en- resting individual. Hypothetically, the orange sig- joy the advantage of Müllerian selection provided nal may thus carry the message that the insect is they display in common any one conspicuous fea- unprofitable, and the underlying defence may then ture”. This applies well to the combined signal- ling behaviour of Aglais and Archiearis, in which consist of two components: distastefulness and the most conspicuous visual feature, the orange rapid movement. wing coloration, seems to have converged to a It could also be argued that the orange signal spectacular degree. shown by Archiearis in flight could be a startle signal analogous to that shown by some larger Acknowledgments. We are grateful to M. 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