Lepidoptera: Lycaenidae) Author(S): Lucas A

Natural History, New Records, and Notes on the Conservation Status of Cyanophrys bertha (Jones) (Lepidoptera: Lycaenidae) Author(s): Lucas A. Kaminski, Sabrina C. Thiele, Cristiano A. Iserhard, Helena P. Romanowski, and Alfred Moser Source: Proceedings of the Entomological Society of Washington, 112(1):54-60. 2010. Published By: Entomological Society of Washington DOI: 10.4289/0013-8797-112.1.54 URL: http://www.bioone.org/doi/full/10.4289/0013-8797-112.1.54

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NATURAL HISTORY, NEW RECORDS, AND NOTES ON THE CONSERVATION STATUS OF CYANOPHRYS BERTHA (JONES) (LEPIDOPTERA: LYCAENIDAE)

LUCAS A. KAMINSKI,SABRINA C. THIELE,CRISTIANO A. ISERHARD, HELENA P. ROMANOWSKI, AND ALFRED MOSER

(LAK) PPG-Ecologia, Instituto de Biologia, Universidade Estadual de Campinas, C.P. 6109, Campinas SP Brazil 13.083-970 (e-mail: lucaskaminski@ yahoo.com.br); (SCT) Departamento de Biologia e Quı´mica, Universidade Regional do Noroeste do Estado do Rio Grande do Sul—Campus Santa Rosa, RS 344—km 39, C.P. 489, Santa Rosa RS Brazil 98900-000 (e-mail: sabrina. [email protected]); (CAI, HPR) PPG-Biologia Animal, Departamento de Zoologia, Universidade Federal do Rio Grande do Sul, Avenida Bento Gonc¸alves, 9500, Porto Alegre RS Brazil 91.501-970 (e-mail: CAI [email protected], HPR [email protected]); (AM) Avenida Rotermund 1045, Sa˜o Leopoldo RS Brazil 93.030-000 (e-mail: [email protected])

Abstract.—The natural history of the potentially threatened hairstreak butterﬂy Cyanophrys bertha (Jones) is discussed, and the morphology of its penultimate and last instar larvae and pupa are described and illustrated. New distribution records from southern Brazil are provided. Based on morphological and ecological traits of immatures and adults, the conservation status of this species is discussed and compared with other sympatric Eumaeini. Key Words: Atlantic rainforest, Conura, ﬂorivory, host plant, immature stages, IUCN Red List, myrmecophily, Neotropical, parasitoids DOI: 10.4289/0013-8797-112.1.54

The Brazilian Atlantic rainforest has mountains from 15 to 238S latitude been considered a hotspot of diversity, (Brown and Freitas 2000). characterized by high levels of ende- Cyanophrys bertha (Jones), an en- mism—about 50% overall and more demic hairstreak butterﬂy of the Atlan- tic rainforest, has been recorded in than 95% in some groups (Brown and moist evergreen and seasonal deciduous Brown 1992). Despite this, the last forests in the coastal mountains of remaining forests continue to be under southern Brazil from 800 to 1,400 m severe anthropogenic pressure (More- elevation (Robbins and Duarte 2005). llato and Haddad 2000). For butterﬂies, This species has been listed as ‘‘vulner- the highest species richness document- able’’ in the IUCN Red List (see Brown ed for this biome occurs in the coastal 1993, 1996; Gimenez Dixon 1996; Mielke and Casagrande 2004). Recent- * Accepted by Robert R. Kula ly, Robbins and Duarte (2005) pub- VOLUME 112, NUMBER 1 55

Figs. 1–7. Some of the life phases of Cyanophrys bertha on its host plant Pyrostegia venusta.1, Inflorescence of P. venusta, scale bar ¼ 1.0 cm; 2, Freshly emerged adult, scale bar ¼ 1.0 cm; 3, Penultimate instar, scale bar ¼ 0.8 mm; 4, Last instar in lateral view, scale bar ¼ 1.4 mm; 5, Last instar in frontal view, scale bar ¼ 1.4 mm; 6, Pupa immediately after molting, scale bar ¼ 0.8 mm; 7, Pupa one day after pupation, scale bar ¼ 0.8 mm. 56 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON lished a phylogenetic analysis and a Santa Rosa County (’3km)and synopsis of the genus Cyanophrys, surrounded by a mosaic of pastures including comments on the relatively and plantation land; the entire area basal position of C. bertha and its originally was covered by Subtropical conservation status. Atlantic Forest (seasonal deciduous Only 13 museum specimens of C. Atlantic Forest). bertha are known (listed in Robbins and All inflorescences of Pyrostegia ve- Duarte 2005) from seven localities in nusta (Ker-Gawl.) Miers (Bignonia- four Brazilian States: two from Minas ceae) (Figs. 1–2) within the study area Gerais, one from Saõ Paulo, three from were inspected. Two penultimate instar Parana´, and one from Santa Catarina. and one last instar larvae of C. bertha Two published records from the States were discovered and taken to the of Rio de Janeiro (Brown 1993) and Rio laboratory for measurements and anal- Grande do Sul (Draudt 1919–1920) are yses. These larvae were reared in plastic not confirmed by voucher specimens containers (about 400 ml) with fresh (Robbins and Duarte 2005). Beyond cuttings of P. venusta with floral buds. these museum specimens and a few Containers were cleaned daily, and food notes on adult reproductive and feeding was offered ad libitum. Shed head behavior (Brown 1993), no information capsules and pupal exuvia were pre- is available about the natural history of served for measurements. Vouchers of this species. the immature stages and parasitoids Because such data are essential for were deposited at the Museu de Zoo- understanding the population dynamics logia (ZUEC), Universidade Estadual of any species and can be important for de Campinas, Campinas, Saõ Paulo, developing conservation strategies of Brazil. endangered butterflies such as C. bertha Morphology.—Measurements were (e.g., Otero and Brown 1986, Francini made using a micrometric scale mount- et al. 2005), we provide novel informa- ed in a Leicat MZ7.5 stereomicro- tion on the natural history and general scope. This scope also was used to morphology of the early stages of C. examine details of the external mor- bertha. Moreover, we report four new phology. The head capsule width of distribution records of this species from larvae is the distance between the most southern Brazil, confirming its occur- external stemmata (as described in rence in the state of Rio Grande do Sul, Freitas 2007). Larval and pupal lengths and discuss the current conservation were taken by measuring in dorsal view. status of this species by comparing it Color patterns in vivo of immature with other sympatric Eumaeini species. stages were captured using a Samsungt L100 digital camera. Morphological MATERIALS AND METHODS terminology follows Stehr (1987) for Collection and rearing.—Observa- larvae, Duarte et al. (2005) for pupae, tions on C. bertha and the collection and Fiedler (1991) for ant-organs. of immature stages were conducted from July to August 2008 in a small RESULTS secondary forest fragment (’24 ha.) on Natural history of Cyanophrys ber- the campus of Universidade Regional tha.—Larvae are solitary and florivo- do Noroeste do Estado do Rio Grande rous, feeding on reproductive tissue of do Sul (278510S, 548290W; 312 m P. venusta, a common Neotropical vine a.m.s.l.), Santa Rosa, Rio Grande do which blooms from the beginning of Sul, Brazil. This fragment is close to May to September in southern and VOLUME 112, NUMBER 1 57 southeastern Brazil (Gobatto-Rodrigues length 0.93–1.19 cm (n ¼ 3), width at and Stort 1992). Each larva fed on the A1 0.41–0.54 cm (n ¼ 3). bud with its retracted head extended New records.—PARANA´ :1/,Pieˆn, into the plant tissue. We did not observe Trigolaˆndia, 900 m, 22 March 2007, I. symbiotic interactions with ants. The Rank & A. Moser leg. (DZUP, Uni- last instar lasted seven days (n ¼ 2); versidade Federal do Parana´, UFPR, pupation lasted 18 days (n ¼ 1). Two Curitiba, PR, Brazil). RIO GRANDE DO larvae were parasitized by wasps of the SUL:1?, Derrubadas, Turvo State Park, genus Conura Spinola (Hymenoptera: 350 m, January 2006, C. A. Iserhard Chalcidoidea); the wasps emerged from leg. (CLDZ, Coleçaõ de Lepidoptera do the pupae. Departamento de Zoologia, Universi- Immature stages of Cyanophrys ber- dade Federal do Rio Grande do Sul, tha.—Penultimate instar larva (Fig. 3): UFRGS, Porto Alegre, RS, Brazil); 1?, Onisciform with hypognathous head Nova Petro´polis, 750 m, 16 January retracted beneath thorax. Body divi- 2005, A. S. Prestes & A. Moser leg. sions inconspicuous, without dorsal (CLAM, Collection of Lepidoptera projections. Head light brown, protho- Alfred Moser, Saõ Leopoldo, RS, racic shield white, body whitish green Brazil); 1?, Santa Rosa, Campus UNI- with two cream bands, one lateral and JUI, 312 m, 31 August 2008 (ex-larva), one subdorsal, spiracles brown. Tegu- S. C. Thiele leg. (MZSP, Museu de ment covered by short translucent setae Zoologia, Universidade Estadual de Saõ and some conspicuous darker setae in Paulo, Saõ Paulo, SP, Brazil). dorsal area. Head capsule width 0.76 mm (n ¼ 2); maximum total length 7.09 DISCUSSION mm. The early stages of C. bertha are Last instar larva (Figs. 4–5): Mor- similar to those of other known Eu- phology similar to penultimate instar; maeini in terms of general morphology body without dorsal projections. Head and biology. The larva is typically light brown, prothoracic shield white, florivorous with an onisciform body and body uniformly light green, spira- and a retracted head, and the pupa lacks cles light brown. Tegument covered by tubercles and is attached to the substrate short yellowish setae with some groups by a silken girdle. The last instar larva of black setae in dorsal area. Dorsal of C. bertha has a smoother body than nectary organ on 8A abdominal seg- the more derived and common species ment, but functionality untested. Head of Cyanophrys (according to the phy- capsule width 1.36–1.40 mm (n ¼ 3), logeny proposed in Robbins and Duarte maximum total length 1.18 cm. 2005). The latter have well-developed Pupa (Figs. 6–7): Color initially dorsal tubercles and setae, e.g., Cya- translucent light green, eventually turn- nophrys acaste (Prittwitz) (L. A. Ka- ing brown with some irregular dark minski unpubl.) and Cyanophrys miser- brown areas. Tegument covered by abilis (Clench) (see Ballmer and Pratt several black setae. Spiracles white, 1992: 44, fig. 18). In Lycaenidae and elliptical, in uniform row. Silken girdle Riodinidae, the development of tuber- around pupa at second abdominal cles or scoli probably is related to segment. Intersegmental areas between defense against natural enemies in A5–6 and A6–7 functioning as stridu- nonmyrmecophilous species (see Ka- latory organ. Segment A10 with ven- minski 2008a, Kaminski et al. 2009); trally flat cremaster comprised of sev- i.e., the loss of myrmecophily in eral short hooked setae. Total body Eumaeini seems to be accompanied by 58 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON the development of dorsal tubercles and under investigation (S. C. Thiele and L. the appearance of scoli (L. A. Kaminski A. Kaminski unpubl.). These data unpubl.). It would be interesting to suggest that characteristics related to determine whether this pattern occurs the natural history of the immature in Cyanophrys and related genera since stages of C. bertha, such as suscepti- there are no records of symbiotic bility to parasitoids, may be related to interactions with ants in these lineages the rarity of the species. However, of Eumaeini. Additionally, experiments further studies are necessary to evaluate examining ant-organ function and larval whether the pattern observed locally is sound production are necessary to consistent over broader temporal and clarify whether myrmecophily is an spatial scales. issue for these Eumaeini lineages (see The Red List of Threatened Species DeVries 1990, Kaminski 2008b). of Rio Grande do Sul (Specht et al. Pyrostegia venusta, the only recorded 2003) does not include any butterfly host for C. bertha, is an abundant plant species. The present findings show that in southern and southeastern Brazil, C. bertha is present but rare in the RS occurring mainly at the edges of and illustrates the need for greater primary and secondary forest fragments sampling of butterflies in the state. and along roads (Lorenzi 2000). Fur- Future revision of the Red List of thermore, host plant records for Cya- Threatened Species of Rio Grande do nophrys and other Eumaeini suggest a Sul should include the listing of C. pattern of polyphagy (Chew and Rob- bertha. The RS is located in a transition bins 1984, Robbins and Duarte 2005, zone between tropical and subtropical Beccaloni et al. 2008; L. A. Kaminski climates, with some ecosystems that unpubl.). Taken together, these two deserve conservation priorities (see features suggest that host plant con- Morais et al. 2007). Previous C. bertha straints are unlikely to be the main records in southeast Brazil were in cause for the rarity of C. bertha. On the mountain habitats over 800 m high other hand, larval competition with (Robbins and Duarte 2005). The occur- other florivorous Eumaeini species, as rence of C. bertha at lower elevations in well as susceptibility to natural ene- the RS is related to latitude, which in mies, may be plausible hypotheses. For turn may promote a subtropical climate example, inflorescences of P. venusta and consequently the occurrence of are used by at least two other common montane species at lower elevations. and widespread species of Eumaeini in The same principle may explain a the study site: Parrhasius polibetes record of C. bertha from the province (Stoll) and Michaelus thordesa (Hewit- of Misiones, Argentina (Bustos 2008). son) (S. C. Thiele and L. A. Kaminski Ecosystems in southern Brazil such as unpubl.). Larvae of P. polibetes (n ¼ 19) that in Rio Grande do Sul support and M. thordesa (n ¼ 5) were recorded peculiar butterfly faunas with potential- during the same period and on the same ly endangered, endemic species that host plants as C. bertha, and none of the should be considered for conservation. former two were parasitized. The sym- This is particularly important for Ly- biotic interactions of P. polibetes and caenidae and Riodinidae given that M. thordesa with ants could explain the many species in those butterfly families lower level of parasitism as compared are rare, highly seasonal, and frequently to C. bertha. Moreover, M. thordesa undetected by collectors (Brown 1993). larvae developed inside inflorescences, More than 20 years of observations a possible defense strategy currently on Lycaenidae lead us to conclude that VOLUME 112, NUMBER 1 59

C. bertha is a rare species, previously bertha and Ayres Menezes Jr. for observed only on mountain slopes of identifying parasitoids. We are grateful the Atlantic Rainforest. Recently, this to the following for critically reading butterfly has been recorded with some the manuscript: Keith S. Brown Jr., frequency from sites in the mountainous Andre´ V. L. Freitas, Daniela Rodrigues, region of southern Minas Gerais to the Robert K. Robbins, and Carla M. Penz. boundary of Saõ Paulo and Rio de We thank CNPq for the doctoral Janeiro states (O. H. H. Mielke and A. fellowship to LAK (Proc. 140183/ Moser unpubl., K. S. Brown Jr. pers. 2006-0). This work was partially sup- comm.). In these localities C. bertha ported by the CNPq (Proc. 478787/ was observed at the edges of primary 2001-4). and secondary forest fragments, often surrounded by sparse pasture and plan- LITERATURE CITED tation land. Biological features, such as Ballmer, G. R. and G. F. Pratt. 1992. Lorantho- susceptibility to natural enemies and mitoura, a new genus of Eumaeini (Lepi- restricted geographic distribution, and doptera: Lycaenidae: Theclinae). Tropical collecting biases (e.g., the species flies Lepidoptera 3: 37–46. only in the forest canopy, and there is a Beccaloni, G. W., S. K. Hall, A. L. Viloria, and conspicuous lack of local butterfly G. S. Robinson. 2008. Catalogue of the inventories) may explain in part the hostplants of the Neotropical Butterflies / ´ ´ scarcity of this species in collections. Catalogo de las plantas huesped de las mariposas Neotropicales. In m3m—Mono- More information on the biology of C. grafias Tercer Milenio, Vol. 8. S.E.A., bertha and the development of a RIBES-CYTED, The Natural History Muse- distribution model for this species are um, Instituto Venezolano de Investigaciones needed to support its conservation Cientı´ficas, Zaragoza, Spain. status and aid in the selection of areas Brown, K. S., Jr. 1993. Selected Neotropical for protection (e.g., Uehara-Prado and species, pp. 146–149. In T. R. New, ed. Fonseca 2007). Although C. bertha Conservation Biology of Lycaenidae (But- terflies). IUCN, Gland, Switzerland. recently was excluded from the official ———. 1996. Conservation of threatened spe- list of endangered species of Brazil cies of Brazilian butterflies, pp. 45–62. In S. (Machado et al. 2008), its rarity and A. Ae, T. Hirowatari, M. Ishii, and L. P. limited distribution across gradients Brower, eds. Decline and Conservation of between tropical and subtropical envi- Butterflies in Japan III. Lepidopterological ronments indicates that it is a potential Society of Japan, Osaka, Japan. indicator of other locally endemic Brown, K. S., Jr. and G. G. Brown. 1992. Habitat alteration and species loss in Brazilian species that are threatened by habitat forests, pp. 119–142. In T. C. Whitmore loss in this transition zone. and J. A. Sayer, eds. Tropical Deforestation and Species Extinction. Chapman and Hall, ACKNOWLEDGMENTS London, England. Brown, K. S., Jr. and A. V. L. Freitas. 2000. We thank the Departamento de Flor- Atlantic Forest butterflies: indicators for estas e A´ reas Protegidas (DEFAP-RS) landscape conservation. Biotropica 32: for allowing us to work in Turvo State 934–956. Park and the Instituto Brasileiro do Bustos, E. O. N. 2008. Diversidad de mariposas Meio Ambiente e dos Recursos Natur- diurnas em la reserva privada Yacutinga, Provıńcia de Misiones, Argentina (Lepidop- ais (IBAMA) for providing collecting tera: Hesperioidea y Papilionoidea). Tropical permits. We thank Keith S. Brown Jr. Lepidoptera Research 18: 78–87. and Olaf H. H. Mielke for providing Chew, F. S. and R. K. Robbins. 1984. Egg-laying comments on the distribution of C. in butterflies, pp. 65–79. In R. I. Wane- 60 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

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