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(ᖪ 25: 1-7 (2005ٿέ៉ Formosan Entomol. 25: 1-7 (2005)

A Newly Discovered Host Association and Descriptions of Immature berenice leei Hsu (: )

Yu-Feng Hsu! Department of Life Science, National Taiwan Normal University, Taipei, Taiwan 116, R. O. C. Ping-Shih Yang*! Department of Entomology, College of Bioresources and Agriculture, National Taiwan University, Taipei 106, Taiwan, R. O. C.

ABSTRACT

An investigation on the immature biology of butterflies on Orchid Island (Lanyu in Chinese), Taiwan was carried out while executing a monitoring program on the effects of exotic, invasive to this small island. Immatures of leei, a recently discovered lycaenid, were found during the investigation. The recognized larval host is Rourea minor of the Connaraceae, a plant family previously unknown as a host for populations of N. berenice from the other regions.

Key words: , host plant, Connaraceae

Introduction successful establishment on the island by exotic species have been documented (Lu There seems to be a tendency for an and Hsu, 2002; Hsu et al., 2003), there is increase in the successful establishment concern that the original fauna may be of exotic species of butterflies in Taiwan negatively affected by such exotic (Chiba and Hsu, 2003; Hsu et al., 2003). invasive species. In order to assess the Although invasive exotic species have effects that exotic species may cause, it been found throughout the island, Orchid seems crucial to have a better unders- Island (Lanyu in Chinese), a small tanding of the biology of the original tropical island off the southeastern coast fauna on Orchid I. A project for of Taiwan, has been a focus of concern. monitoring exotic butterflies which have The reason why Orchid I. is of particular invaded the island was initiated in 2003, interest is due to the fact that the island and an investigation on gathering hosts a diversity of butterflies that biological information is simultaneously greatly differ from that of the main being carried out. Findings during the island of Taiwan, including species like project include the discovery of the Troides magellanus, which is considered immature biology and host association of endangered locally and internationally Nacaduba berenice leei Hsu. (Yen and Yang, 2001). As recent cases of Nacaduba berenice leei (Fig. 1.1) is

*Correspondence address e-mail: [email protected] ! Host Association and Immatures of Nacaduba berenice leei 1 one of the most recently described philippinensis (Ulmaceae), and Trema butterflies in Taiwan (Hsu, 1990). orientalis (Ulmaceae) were examined for Although the species N. berenice is the presence of immature Nacaduba widespread throughout Southeast Asia berenice leei. No sign of immatures of and (Tite, 1963), to the present this lycaenid, however, was found from it has only been found on Orchid I. any of above plants after 15 months of within Taiwan. The present study investigation. Alternatively, ova and confirms the host plant of N. berenice leei larvae of N. berenice leei were found from on Orchid I.; an account on the immatures young shoots of Rourea minor of this lycaenid is also given. (Connaraceae) (Fig. 1.2) and subsequently reared out during the investigation (HSU Materials and Methods 03F8; 04H5).

Plants that are potentially utilized Accounts of immatures of Nacaduba by larva of N. berenice leei were berenice leei Hsu, 1990 examined on Orchid I. during the investigation; these included plants in Ovum (Fig. 1.3): 0.45 ± 0.01 mm in various families, e.g., the Sapindaceae, diameter, 0.22 ± 0.01 mm in height (n = Sterculiaceae, Fabaceae, and Ulmaceae 10). Mandarin-shaped, pale olive, semi- according to host records from regions transparent in color; chorion with white other than Orchid I. (Bell, 1918; Common ridges forming network with diamond- and Waterhouse, 1981; Parsons, 1991, shaped pattern laterally and irregular 1999; Kitamura, 1994, 2001; Braby, 2000; sculpturing on top. Robinson et al., 2001; Herbison-Evans and Crossley, 2003). Collected immatures Larva (Figs. 1.4, 1.5) were brought back to a laboratory on the First instar larva (Fig. 1.4): Body campus of National Taiwan Normal smooth with transparent primary setae, University, Taipei for subsequent obser- pale olive right after hatching. Head pale vations. Rearing records adopted the brown, glossy, with brown stemmata. system used by Powell and De Benedictis Legs and prolegs pale olive. Caudal end (1995). Each collection of immatures was of anal plate circular. Body turning green labeled according to the collection year or orange after feeding. Arrangement of and month: e.g., 03F8 refers the eighth primary setae as follows: XD1 and XD2 collection in June 2003. This system very short but equally long, barely employs alphabetical letters to represent recognizable. D group unisetose, only months in sequence. elongate, setaceous D2 present on T1 The terminology for the myrmeco- through T3, A1 through A8 all pointed philous organs follows Fiedler (1991). posteriad; well separated on T1 and T2, close to dorsal midline on T1 and A1 Results through A8. SD and L setae vestigial. SV setae short, transparent, arranged on the During the survey, vegetation of same plane throughout body. Three SV Pometia pinnata (Sapindaceae), Cardios- setae present on T1 through T3, 2 on A1 permum halicacabum (Sapindaceae), through A8. Four SV setae present on A Dendrolobium umbelatum (Fabaceae), 9 + 10. Derris oblonga (Fabaceae), Derris trifoliata Second instar larva: Head green. (Fabaceae), Ormocarpum cochinchinense Coloration of body variable, being pale (Fabaceae), Pueraria montana (Fabaceae), green, orange, or red. Sterculia ceramica (Sterculiaceae), Celtis Third instar larva: Body relatively

ௐ˘ഇס̣˩˟ᖪௐٿέ៉ 2 Fig. 1. 1. An adult of Nacaduba berenice leei taking nectar. 2. Host plant (Rourea minor) of Nacaduba berenice leei on Orchid I. 3. Ovum of Nacaduba berenice leei on a new bud of Rourea minor. 4. First instar larva of Nacaduba berenice leei. 5. Mature larva of Nacaduba berenice leei. 6. Pupa of Nacaduba berenice leei in debris. stout, with a medial depression in thorax weakly sclerotized. Body cream yellow dorsally. Body covered with short, trans- with red markings present laterally and parent setae. Functional DNO and TOs dorsally. Spiracles same color as body. both present. T1 shield ladder-shaped, Fourth (last) instar larva (Fig. 1.5):

Host Association and Immatures of Nacaduba berenice leei 3 Similar to 3rd instar, DNO and TOs both investigation for the present study. present. T1 shield diamond-shaped, green. Instead, ova and larvae of N. berenice leei Body covered with asteroid setae; setaceous, were found on young growth of Rourea elongate setae present below spiracles. minor (Connaraceae), a woody vine Coloration of body variable, with ground widespread in the forests there (Cheng color ranging from pale green or yellow and Lu, 2000; Liu et al., 2001). to pale red. Prominent red markings of An association with the Connaraceae variable extent present dorsally and is rare among lycaenid butterflies. In a laterally, forming longitudinal line above worldwide analysis on the relationship and below spiracles and mediodorsally. between lycaenids and families of host Spiracles cream yellow. Larva reaching plants they utilize, Fiedler (1995) did not 11.04 ± 0.40 mm in length upon matu- even include this plant family. Robinson ration (n = 10). et al., (2001) recognized only five species Pupa (Fig. 1.6): Of typical lycaenid that are known to be associated with the form. Surface with creases, glossy; color Connaraceae in the Oriental region; brown tinged with yellow, mottled with nevertheless, among them, four are dark brown, forming a longitudinal known as polyphagous species, with just medial band dorsally. Spiracles brown. Nothodanis schaeffera recognized as a specialist. Braby (2000) listed three Bionomics Australian lycaenid species that are The ovum is laid on young growth associated with the Connaraceae, but (Fig. 1.3). The enclosed larva feeds only again two of them are general feeders; on soft tissues of the host plant, such the other one, viz. Danis danis, is a young leaflets or stems. No myrmecophily specialist on the Connaraceae and Faba- was observed. Pupation occurs in debris ceae. The only other known Connaraceae in a cavity (Fig. 1.6). specialist is Nacaduba sericina from the Vouchers: 3 ♂, 2 ♀, TAIWAN: TAI- (Kitamura, 2001). Thus the DONG Co., Orchid I. (Lanyu), Sidaogou, Connaraceae association by N. berenice 13/15-VI-2003, Coll. Y. F. Hsu, emgd. leei at Orchid I. represents an unusual 28-VI/4-VII-2003, reared from Rourea host-association among lycaenid butter- minor, HSU 03F8; 14 ♂, 12 ♀, TAIWAN: flies. TAIDONG Co., Orchid I., Badaiwan, 6/8- So far the distributional range of N. VIII-2004, Coll. Y. F. Hsu, emgd. 17-VIII/ berenice leei includes only Orchid I. and 23-VIII-2004, reared from R. minor, HSU the Philippines (Takanami and Seki, 04H5. 2001). As noted previously, populations of N. berenice leei in the Philippines are Discussion known to use N. mutabile of the Sapindaceae as a host plant (Kitamura, The other populations of N. berenice 1994; 2001). Plants in this plant family leei are found in the Philippines are extensively utilized as larval hosts by (Takanami and Seki, 2001), where the other subspecies of N. berenice leei in host plant of N. berenice leei is known to regions other than Orchid I. and the be Nephelium mutabile [mis-spelt as Philippines. The known host plants of N. mutabili] (Sapindaceae) (Kitamura, 1994; berenice from other regions include 2001). Although plants in the Sapin- Alectryon coriaceus, Arytera divaricata, daceae are abundant on Orchid I. (Cheng Ar. foveolata, Ar. pauciflora, Atalaya and Lu, 2000), no immatures of N. salicifolia, Cupaniopsis anacardioides, C. berenice leei were found from these plants parvifolia, Elattostachys microcarpa, E. after extensive searching during the nervosa, Heterodendrum diversifolium,

ௐ˘ഇס̣˩˟ᖪௐٿέ៉ 4 and Jagera pseudorhus of the work was supported by a Council of Sapindaceae; Macadamia tetraphylla and Agriculture grant 92AS-1.8.1-BQ-BB. M. integrifolia of the Proteaceae; and Aphananthe philippinensis of the References Ulmaceae in Australia (Common and Waterhouse, 1981; Herbison-Evans and Brady, M. F. 2000. Butterflies of Australia, Crossley, 2003); Calliandra surinamensis Their Identification, Biology and of the subfamily Mimosoideae in the Distribution. CSIRO, Collingwood, xx Fabaceae and Theobroma cacao of the + 976 pp. Sterculiaceae in New Guinea (Parsons, Bell, T. R. 1918. The common butterflies 1991; 1999); and Wagatea spicata of the plains of India, part 20. J. (Fabaceae) in India (Bell, 1918). It is Bombay Nat. Hist. Soc. 25: 636-664. interesting that although several plant Chiba, H., and Y. F. Hsu. 2003. Notes on genera of the Sapindaceae, Sterculiaceae, Taiwanese butterflies. Nat. and Fabaceae grow on Orchid I. (Cheng 38(6): 32-35 (in Japanese). and Lu, 2000), none was found to be a Cheng, H. W., and S. Y. Lu. 2000. Botel host plant of N. berenice leei after Tabaco, Yami & Plants. Lamper extensive field investigations. Conse- Enterprises, Taipei. 268 pp. (in quently the population of N. berenice leei Chinese). on Orchid I. is the first known Common, I. E. B., and D. F. Waterhouse. population of the species that specializes 1981. Butterflies of Australia. Angus on the plant family Connaraceae. & Robertson Publishers, Sydney. xiv Moreover, the N. berenice leei population + 682 pp. on Orchid I. is known to be the Fiedler K. 1991. Systematics, evolutionary, northeastern limit of the distributional and ecological implications of Myrme- range of the species (Hsu, 1990). Some cophily within the Lycaenidae (Insecta: species of Taiwanese butterflies that Lepidoptera: Papilionoidea). Bonn. represent peripheral populations in Zool. Monogr. 31: 1-210. overall geographic distributions of those Herbison-Evans D., and S. Crossley. 2003. species are known to demonstrate mono/ Lepidoptera Larvae of Australia. oligophagy in contrast to the polyphagy Available at http://linus.socs.uts.edu. of the core populations. For instance, the au/~don/larvae/lyca/berenic.html. only reliable host record of Eurema Hsu, Y. F. 1990. The berenice complex of alitha in Taiwan is Galactia tenuiloba of the Nacaduba in Taiwan the Fabaceae (Hsu, 2001), whereas this (Lepidoptera: Lycaenidae). J. Taiwan pierid butterfly demonstrates extensive Mus. 43: 11-17. polyphagy in the Philippines (Kitamura, Hsu, Y. F. 2001. Butterflies of Taiwan, Vol. 1996). The Connaraceae association by N. 2. Fonghuanggu Bird Park, Luku, berenice leei on Orchid I. may be another Taiwan. 383 pp. representative of such a phenomenon. Hsu, Y. F., Y. H. Li, and P. S. Yang. 2003. The current status of exotic butter- Acknowledgments flies in Taiwan. Proceedings of the Symposium on the Management of We thank Shen-Horn Yen (National Invaded Organisms. pp. 138-148 (in Sun Yat-Sen University, Kaohsiung) for Chinese). providing literature relevant to the study. Liu, H. Y., Yang, Y. P., Lu, S. Y., Shih, and Hang-Chi Huang and Yu-Cheng Hsu (the B. L. 2001. Manual of Taiwan Vascular Butterfly Conservation Society of Taiwan, Plants, Vol. 3, II. Spermatophyta, 2. Taipei) assisted with the fieldwork. This Angiosperm, A. Dicotyledons (con-

Host Association and Immatures of Nacaduba berenice leei 5 tinued). The Council of Agriculture, Tortricidae) in the Western United Executive Yuan, Taipei. 389 pp (in States. University of California Chinese). Publications in Entomology 115, Kitamura, M. 1994. On host associations Berkeley, CA. of Philippine butterflies, No. 2, Robinson, G. S., P. R. Ackery, I. J. Lycaenidae (2). TSU-I-SO 768: 1-22 Kitching, G. W. Beccaloni, and L. M. (in Japanese). Hernández. 2001. Hostplants of the Kitamura, M. 1996. The study of Eurema moth and butterfly caterpillars of the alitha (C. & R. Felder) (Pieridae) in Oriental Region. The Natural History the Philippines (2) Diversification of Museum, London. 744 pp. larval feeding habit. Butterflies 15: Stehr, F. W. 1987, Order Lepidoptera. pp. 27-40 (in Japanese). 288-305. In: F. W. Stehr, ed. Immature Kitamura, M. 2001. On host associations Insects. Kendall/Hunt Publishing of Philippine butterflies, No. 45, Company, Dubuque, IA. xiv + 754 Lycaenidae (13). TSU-I-SO 1026: 1-19 pp. (in Japanese). Takanami, Y., and Y. Seki. 2001. A Lu, C. C. 2002. Catopyrops ancyra almora, synonymic list of Lycaenidae (Lepido- a lycaenid butterfly new to Taiwan: a ptera) from Philippines, edition 12. case of biological invasion from the Available at http://www.asahi-net.or. Philippines. BioFormosa 37: 25-30. jp/~EY4Y-TKNM/frontp.html. Parsons, M. 1991. Butterflies of the Tite, G. E. 1963. A synonymic list of the Bulolo-Wau Valley. Bishop Museum, genus Nacaduba and allied genera Honolulu. 280 pp. (Lepidoptera: Lycaenidae). Bull. Br. Parsons, M. 1999. The Butterflies of Mus. (Nat. Hist.) Entomol. 13: 69- Papua New Guinea, Their Syste- 116. matics and Biology. Academic Press, Yen, S. H., and P. S. Yang. 2001. London and San Diego. xvi + 736 pp. Illustrated Identification Guide to Powell, J. A., and De Benedictis, J. 1995. Insects Protected by the CITES and Biological relationships: host tree Wildlife Conservation Law of Taiwan, preferences and isolation by phero- R.O.C. Council of Agriculture, Execu- mones among allopatric and sympatric tive Yuan, Taipei. 179 pp. populations of western Choristoneura. pp. 21-68. In: J. A. Powell, ed. Received: September 7, 2004 Biosystematic Studies of Conifer- Accepted: May 31, 2005 feeding Choristoneura (Lepidoptera:

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Host Association and Immatures of Nacaduba berenice leei 7