Entomologist s Gazette : 3-12.

Entomologist s Gazette 2006 57: 3-12. A review of records for Colias erate (Esper, [1805]) (Lep.: Papilionoidea Pieridae) in Cyprus: were they all yellow forms of Colias croceus (Geoffroy, 1785)? EDDIE JOHN Davies Cottage, Penllyn, Cowbridge, Vale of Glamorgan, CF71 7RQ, Great Britain E-mail: eddie@grayling.dircon.co.uk JOHN G. COUTSIS 4 Glykonos Street, GR-10675 Athens, Greece E-mail: kouts@otenet.gr CHRISTODOULOS MAKRIS Ethnikis Antistaseos 21, 3022 Lemesos, Cyprus E-mail: r.c.makris@cytanet.com.cy Introduction A recently published book Butterflies of Cyprus (Makris, 2003), written by one of the authors of this paper, provisionally includes Colias erate (Esper, [1805]) among 53 species of butterfly recorded for the eastern Mediterranean island of Cyprus. The inclusion was considered admissible following three previously published, and to our knowledge unchallenged, records which embraced C. erate within the Cyprus list (Hofmann & Rose, 1987; Manil, 1990; John, 2000). The capture, in April 2001, of a fourth candidate specimen, provided an opportunity to investigate the true identity of this species but, in practice, this proved to be more exacting than anticipated. The related Colias croceus (Geoffroy, 1785) is a common butterfly in Cyprus and is on the wing throughout all months of the year, with numbers dwindling only during the short winter and at the height of summer. C. erate is known to be expanding its range within Europe and has spread throughout Bulgaria, occurring in NE Greece (van der Poorten et al. 1988) and European Turkey (Hesselbarth et al, 1995; Tolman, 1997; Joseph Verhulst pers. comm.). The April 2001 capture in Cyprus of the yellow Colias referred to in the opening paragraph aroused further speculation but, as Cyprus is well outside the established range of C. erate, its absolute acceptance as C. erate was deferred until further opinion was sought. Although occasional yellow Colias females have been found in Cyprus, we confine our detailed investigations to the genitalia examination of two yellow male Colias: one taken by David Whaley in April 2001 (as illustrated on Pages 128/129 of Butterflies of Cyprus by Christodoulos Makris (CM)) and a second, yellow male kindly provided for examination by Peter Hofmann and previously written up in Hofmann & Rose (1987). In this paper, we also take the opportunity to review all known published records for C. erate in Cyprus, and deliberate on the true identity of a yellow form of Colias that appears infrequently in Cyprus and which has been reported, sometimes incidentally, by various observers over a period of nearly 100 years. Historical data Checklists of species, dating back to the early 1900s, make no specific mention of Colias erate; neither does Parker (1983) in his authoritative account of the island s butterflies. However, Bucknill (1911) and Turner (1920) when commenting on

sightings in Cyprus of Colias croceus state, specimens may be found in which the wings or even only a pair of wings are lemon yellow (Bucknill, 1911) and, The yellow colour also varies in shade, some specimens being quite dark and others almost lemon yellow (G. F. Wilson, in Turner, 1920) and, finally, Several examples, both males and females, are of the pale orange or lemon colour to which the name helicina Obthr., applies. (Turner, 1920). C. erate was first listed as a possible species for Cyprus by Hofmann & Rose (1987). An approximate translation of an extract from their account reads: Hofmann observed very worn specimens near Platres. Since the occurrence of erate in Turkey is uncertain (Wagener pers. comm.), also Lebanon, where only two specimens in one year (1971) have so far been captured, the occurrence of this, principally central- Asiatic species in Cyprus requires further confirmation (migrant or established population?). Peter Hofmann (pers. comm.) advises that he took a male C. erate in June 1984 near the village of Ágios Nikólaos (790 m) on the southern slopes of the Tróodos Mountains. The specimen remains in his collection, though the abdomen was generously submitted to us for examination. While questioning whether the presence of C. erate might be the result of a migration or indeed be an indication of the presence of a resident population, there is no suggestion by Hofmann & Rose of a third possibility - that the butterflies were a yellow form of C. croceus. Whereas various earlier papers were mainly accounts of brief collecting trips, Parker s three-season stay (1973-1975) was significant in terms of the duration of his time on the island, and the depth and accuracy of his data. Yet, this study was known only to a relatively small audience, such that little information on the island s butterflies was widely available. Even within the past decade, entomological museum libraries, in response to requests for general information on the butterfly species to be found in Cyprus, have supplied the much earlier and far less reliable accounts by Bucknill or Turner. Additionally, all popular field guides on European butterflies, while listing Mediterranean islands as far east as Crete and Rhodes, failed to include Cyprus, other than possibly giving an incidental and selective reference (e.g. Tolman, 1997). It was against this background, with C. erate already listed as a possible species for Cyprus, that Luc Manil (1990) was the next to record C. erate in Cyprus, with a reported sighting at Chandriá in June 1989 at an altitude of 1100 m, also in the Tróodos Mountains. Ten years later, one of the authors of this paper, Eddie John (EJ), also published a report of C. erate in Cyprus (John, 2000) following a sighting at the Lárnaka salt lake (0 m) in 1998. However, in neither of these cases was a specimen taken. Luc Manil has since indicated that his field identification of C. erate could have been erroneous (pers. comm. to Rob Parker) and now accepts that it may have been a yellow form of croceus. Similarly, with identification relying on external characteristics only, the erate sighting by EJ must also be regarded as unsustainable. However, the circumstances surrounding this sighting are unusual and worth recording. On 8 September 1998, following an exceptionally hot summer (even for Cyprus), a fresh, strikingly bright, lemon-yellow butterfly was observed at Lárnaka during a period when only one typical and much worn, C. croceus had been seen since 26 July. The appearance was so unlike any of the hundreds of typical croceus seen over the preceding 11 months (when EJ was living in Cyprus), that thoughts were introduced of a possible C. erate migration from Turkey (70 km to the north), Syria or Lebanon (105 km and 165 km respectively to the east). Almost another month was to elapse before C. croceus began to appear in numbers at coastal regions, though it was observed on 13 September 1998 at Kyperoúnta (1200 m) in the Tróodos Mountains.

Occurrence of C. croceus in Cyprus As mentioned earlier, C. croceus is commonly found in Cyprus, though numbers are rarely if ever abundant even in areas where Lucerne (Medicago sativa) is grown as a forage crop (pers. obs. CM & EJ). This is attributable to a general paucity of larval host-plants during the summer breeding season of this polyvoltine species. At best, tens but never hundreds of Colias may be seen at a time. Cyprus receives most of its rainfall during the winter months of December, January and February, when approximately 60% of the annual average precipitation of 480 mm occurs (Makris, 2003). Barely 5% of the annual average rainfall occurs during the summer months with the result that large areas of the island begin to desiccate by May/June. Away from sources of water such as irrigated areas and irrigation channels the ground soon becomes unfavourable for the support of luxuriant plant growth. As a consequence, population numbers of C. croceus are unable to build up and there are no, known, regular migrations to boost the local population. This is in sharp contrast to the Azores island of Faial, for example, where the presence of large numbers of croceus enabled John Tennent to estimate the frequency of a yellow form of C. croceus, f. cremonae, when compared with typical C. croceus (Russell et al., 2003). There, Tennent reports, In suitable places. it was not unusual to see several thousand C. croceus individuals, of which more than a hundred were f. cremonae, during several hours over only a few acres of ground. It was calculated that f. cremonae accounted for an estimated mean ranging up to 6.25% in some coastal populations of C. croceus, with cremonae males far outnumbering females. By contrast, the presence of the yellow Colias in Cyprus is extremely rare indeed, with only two males (those taken by Peter Hofmann & David Whaley) and a similarly low number of females (single specimens taken by CM & David Whaley) known from recent times. Interestingly, the pale female C. croceus f. helice is also less common in Cyprus than in other populations of croceus. Tolman (1997), for example, comments that f. helice, comprises 5-10% of all populations. However, in Cyprus, this percentage appears to fluctuate; in some seasons f. helice numbers approach 10% of the crocea population, whereas in other seasons this figure barely reaches 1-2% (pers. obs. CM & EJ). This is not to suggest that the yellow form, f. cremonae, found in the Azores, is the same as that present in Cyprus. Russell et al. (2003) describe f. cremonae as lemon-yellow, completely lacking in red pigment, with the legs, frons, wing fringes and antennal shaft greenish in hue, but this description does not apply to the yellow Colias from Cyprus, which, wing colour apart, resembles the typical form of crocea in colouration. Russell et al. characterise C. erate as having, a yellow (i.e. not orange) wing colour pinkish legs, frons, antennal shafts and wing fringes In other words, the typical superficial characteristics of Colias erate were present in the yellow male, referred to earlier as the fourth (erate) candidate, which was discovered, on 21 April 2001, as a chance find near Páfos in the west of the island. It was found in the clutches of a spider, probably a crab spider (family Thomisidae) which are well recognized predators of butterflies in Cyprus (Makris, 2003), and was already dead, though relatively little external damage was evident. The butterfly, which was provisionally thought to be C. erate, was sent to EJ for investigation. Preliminary investigation The specimen was immediately forwarded to Otakar Kudrna in Germany, who agreed that there were certain superficial resemblances to C. erate. However, he considered it more likely to be a yellow form of C. croceus, and wished to photograph

the specimen using an ultraviolet light technique to determine if the wings were UVlight absorbent or UV-light reflective. While some workers have less than complete confidence in using this technique as a diagnostic tool, Kudrna (1992) writes, some superficially similar butterfly species can be identified by their distinct hidden wing pattern., and illustrates C. croceus among species that reflect light, whereas C. erate is UV-light absorbent. Moreover, Kudrna (1992) also states, Whereas all European Colias species containing orange males reflect the UV light rays, all yellow males absorb it, the only exception being C. erate which absorbs UV light regardless of its typical yellow or aberrant pale orange ground colour of the dorsal wing surface. Although the photographic results indicated the identity of the specimen to be C. croceus, the photographs, taken under pressure of time, were not of a quality necessary for publication. Kudrna (pers. comm.) comments that the taking of photographs in UV-light is an involved procedure and also demands fresh, perfectly set specimens. Unfortunately, the specimen met neither of these requirements. Furthermore, rapidly advancing deadlines for the completion of his Mapping European Butterflies project (Kudrna, 2002) did not allow him to repeat the technique under more controlled conditions. Hypothetically, it could even be argued that one would also need to include yellow specimens of crocea in order to establish whether they, too, reflect UV light in the same way as the normal orange form, in order to be able to use this characteristic as a reliable identification aid. However, before Otakar Kudrna had the opportunity to continue with the examination the specimen was released to others and here the picture became even more blurred, as some very experienced lepidopterists, including a Colias expert recommended by the Natural History Museum, London, favoured an identity of C. erate (on the basis of external morphology only) while others were equally convinced that the butterfly was a yellow form of C. croceus. The presence of an androconial patch tended to support those in favour of a yellow croceus, but this, in itself, is inconclusive, as a sex brand is also found in a small percentage of erate. Because of the lack of unanimity among expert opinion a cautious approach was taken upon the publication of Butterflies of Cyprus (Makris, 2003), wherein it is stated, Although investigation continues into the occasional presence of Colias erate in Cyprus, the distance from its known range adds doubt to its occurrence here. Further doubt was added when Torben Larsen advised (in pers. comm. to EJ) that he is now of the opinion that the 1971 sightings reported in Larsen (1974), and alluded to by Hofmann & Rose (1987) were, in fact, yellow forms of crocea. This, despite the statement in his book, Status: The two Lebanese specimens in no way differ from nomino-typical erate, the type locality of which is southern Russia. (Larsen, 1974). Consequently, though CM and EJ (the book s editor) tentatively included C. erate among the species listed in Butterflies of Cyprus, the restricted range of this species within Europe remained of prime concern to both. The investigated (Whaley) specimen is shown in the colour plate, along with other Colias from Cyprus:

Row 1: Upperside and underside photographs of the yellow male Colias from Cyprus, leg. David Whaley. Row 2: Lighter forms of female Colias may also be found. No significance should be attached to the small size of this female, as dwarf forms occur in Cyprus (CM and EJ, pers. obs.). Rows 3 and 4: Typical upperside and underside forms of male (Row 3) and female (Row 4) Colias croceus from Cyprus. All specimens are in the collection of C. Makris. Post-publication investigation Following publication, a copy of Butterflies of Cyprus was sent to John Coutsis (JC), who later conveyed his opinion to CM and EJ that the illustrated specimens were yellow forms of C. croceus, rather than C. erate. In further correspondence JC drew attention to Higgins (1975) in which the author refers to a difference in the valvae between erate and croceus, stating for C. erate: "Valve short, posterior border strongly angled below head", and for C. croceus: "Head of valve wide, posterior border evenly curved without an angle." Verhulst (2000) corroborates this finding. In order to confirm these differences, JC examined specimens of erate and croceus from his own collections. Methods The specimens selected were from within accepted, established ranges for both species (see data below) and included possible hybrids. The genitalia drawings were undertaken by means of a Leica MZ7.5 stereomicroscope with drawing tube, the appendages being drawn while immersed in alcohol, free from pressure due to mounting, and therefore undistorted.

Results The specimens, whose valvae were examined in order to produce a standard and to confirm Higgins findings, are detailed under Figs. 1 16 (see Captions). The relevant drawings, which show a side view of the exterior face of the left valva, do, indeed, confirm a difference between C. erate and C. croceus as indicated by Higgins (1975). In C. erate the distal border of the valva is strongly angled, whereas in C. croceus it is smoothly curved, almost spatulate in shape. As can be seen from the drawings, this diagnostic feature is consistently and reliably present throughout all specimens. Accordingly, the fourth candidate specimen tentatively thought to be C. erate from Cyprus, was despatched to JC for similar examination. The result, as shown in Fig. 11, shows the valva of the Cypriot specimen to be characteristic of C. croceus, not C. erate. In view of this result, an enquiry was made to have the original (Hofmann) specimen submitted for similar examination. This, too, revealed the specimen to have valva typical of C. croceus, as shown in Fig. 12. Conclusion In view of the foregoing (and in the absence of specimens) the field observations of C. erate reported by Manil (1990) & John (2000) cannot be substantiated and should be considered invalid. The only two specimens of Colias erate (males) known to have been taken have here been shown to be a yellow form of Colias croceus. Our findings coincide with those of D. van der Poorten et al. (1988), who in their paper describing the finding of C. erate in NE Greece, also refer to the presence of a yellow form of C. croceus, which can easily be mistaken for C. erate without examination of the genitalia. Especially the yellow form of C. croceus, known as f. erateformis Niculescu, closely resembles C. erate. In discussing the findings of the genitalia examination, the authors further state, The valvae of C. croceus, f. erateformis were found to be identical to those of typical C. croceus. Thus it becomes evident that the conservative record for C. erate in Cyprus, as listed in Makris 2003, should be withdrawn in favour of Colias croceus f. erateformis. Acknowledgements The authors are grateful to Martin Honey (BMNH), Torben Larsen, Luc Manil, Rob Parker, Peter Russell, John Tennent, Joseph Verhulst and Bob Worthy for their assistance in this investigation; also to the late Jan Haugum. David Whaley kindly provided the Colias specimen that led to this enquiry, and we are particularly grateful to Otakar Kudrna for his helpful investigations and to Peter and Maike Hofmann for their willing cooperation in releasing their Colias specimen for examination. We also gratefully acknowledge the financial assistance of The A. G. Leventis Foundation who sponsored the colour plate. References Bucknill, J. A. S. 1911. The Butterflies and Moths of Cyprus. English School Magazine, Nicosia. Hesselbarth, G., van Oorschot, H. & Wagener, S. 1995. Die Tagfalter der Türkei. Vols 1 & 2: 1354pp., Vol 3: 847pp. Bocholt.

Higgins, L. G. 1975. The Classification of European Butterflies, 320 pp. London. Hofmann, P. & Rose, K. 1987. Zur Rhopaloceren-Fauna Zyperns. Nachrichten des entomologischen Vereins Apollo, Bd. 7, Heft 4: 133-141. John, E. 2000. Butterflies of Cyprus 1998 (Records of a year s sightings). The Bulletin of the Amateur Entomologists Society, Pamphlet No.15:46 pp. Kudrna, O. 1992. On the hidden wing pattern in European species of the genus Colias Fabricius, 1807 (Lepidoptera: Pieridae) and its possible taxonomic significance. Entomologist s Gazette 43: 167-176. 2002. The Distribution Atlas of European Butterflies. Oedippus, Nr. 20. 343pp. Schweinfurt. Larsen, T. B. 1974. Butterflies of Lebanon 255pp. Beirut. Makris, C. 2003. Butterflies of Cyprus. 329pp. Nicosia. Manil, L. 1990. Les Rhopalocères de Chypre. Linneana Belgica XII (8): 313-391. Parker, R. 1983. The Butterflies of Cyprus. Entomologist s Gazette 34: 17-53. Poorten, D. van der, Dils, J. & Coutsis, J. G. 1988. Colias erate (Esper, 1804), a true resident of the Greek butterfly fauna (Lepidoptera: Pieridae). Phegea 16 (4): 123 127. Russell, P. J. C., Tennent, W. J., & Hall, D., 2003. Polymorphism in Colias croceus (Geoffroy, 1785) (Lepidoptera: Pieridae) from the Azores, with a description of a new form and notes on its frequency, genetics and distribution. Entomologist s Gazette 54: 143-152. Tolman, T. & Lewington, R. 1997. Butterflies of Britain & Europe. 320pp. London. Turner, H. J. 1920. The Butterflies of Cyprus. Trans. Ent. Soc. Lond. 1920: 170-207. Verhulst, J. 2000. Monograph of the Genus Colias, 2 Vols., 308 pp., 183 plates. Keltern, Germany. Addendum Since writing this paper we have been advised of two further yellow Colias croceus (both males) held in the collection of Michel Morisseau, a geologist who has lived, worked and collected enthusiastically in Cyprus since 2000. These, along with one other observed in flight, represent the only yellow forms (out of many hundreds of typical croceus) seen by Morisseau during this five - year period, thus providing a further indication of the infrequency with which this form is encountered in Cyprus. They were collected at Athalassa (Nicosia) on 6 April 2003 and the Avakas Gorge (Paphos) on 29 April 2004, and although neither has been submitted for genitalia examination the presence of androconia on both specimens strongly indicates that they are also Colias croceus f. erateformis.

Captions to Figs. 1-16 Figs. 1 16. Side view of outer face of left valva of Colias species. C. erate (Figs. 1 5) 1 Yellow, without sex brand. Genitalia Prep. No.: 3791. Russia, Sarepta, Saratov, 100 m, 18.viii.1981. 2 Yellow, without sex brand. Genitalia Prep. No.: 3792. Russia, Sarepta, Saratov, 100 m, 27.viii.1981. 3 Yellow, without sex brand. Genitalia Prep. No.: 3794. Greece, Makedonía, Dráma district, 30 km along road from Dráma to Vólax, ca. 800 m, 12.vi.1984. 4 Yellow, without sex brand. Genitalia Prep. No.: 1794. Greece, Makedonía, Dráma district, 30 km along road from Dráma to Vólax, ca. 800 m, 12.vi.1984. 5 Yellow, with sex brand. Genitalia Prep. No.: 3796. Russia, Sarepta, Saratov, 100 m, 31.viii.1981.

C. croceus (Figs. 6 13) 6 Orange, with sex brand. Genitalia Prep. No.: 1796. Greece, Spétses island, 26.v.1963. 7 Orange, with sex brand. Genitalia Prep. No.: 3790. Greece, Spétses island, 14.v.1963. 8 Orange, with sex brand. Genitalia Prep. No.: 3793. Greece, Makedonía, Rodópi Mts., 1000-1200 m, 10.vii.2000. 9 Orange, with sex brand. Genitalia Prep. No.: 3797. Greece, Stereá Ellás, Delfí, ca. 600 m, 7-8.vii.1998. 10 Yellow, with sex brand. Genitalia Prep. No.: 2494. Greece, Lésvos island, Eressós, 23.v.1988. Whaley specimen: 11 Yellow, with sex brand. Genitalia Prep. No.: Prep. No. 3805. Cyprus, Páfos, Ármu, 300 m, 21.iv.2001. Hofmann specimen: 12 Yellow, with sex brand. Genitalia Prep. No. 3808. Cyprus, Ágios Nikólaos, Tróodos Mt., 900 m (South side), 30.v 12.vi.1984. 13 Yellow, with sex brand. Genitalia Prep. No.: 1798. Greece, Makedonía, near Véria, 22.vi.1986. 14 Yellow-orange, with sex brand. Genitalia Prep. No.: 1795. Greece, Makedonía, Dráma district, 30 km along road from Dráma to Vólax, ca. 800 m, 14.vi.1987. Probable hybrids between C. erate and C. croceus (Figs. 15, 16) 15 Yellow with orange wash, without sex brand. Genitalia Prep. No.: 3795. Russia, Sarepta, Saratov, 24.vii.1983. 16 Yellow with orange wash, without sex brand. Genitalia Prep. No.: 1797. Greece, Makedonía, Dráma district, 30 km along road from Dráma to Vólax, ca. 800 m, 26.vi.1987.