Larval cryptic coloration and mistletoe use in the metalmark butterfly Dachetola azora (Lepidoptera: Riodinidae).
Key words: Lasaia, Loranthaceae, Metacharis, mistletoe-feeding, scanning electron microscopy.
Aside from being a highly diverse butterfly family, Riodinidae is historically one of the least known families of Neotropical butterflies (see DeVries, 1997). Although the knowledge of the systematics and taxonomy of this group have increased considerably over the last three decades (e.g., Harvey, 1987; Callaghan and Lamas, 2004; Hall, 2005; Penz and DeVries, 2006; Dolibaina et al., 2013), the natural history and morphology of immature stages are unknown for the majority of the over one hundred described riodinid genera. A good example of this lack of knowledge occurs in Dachetola Hall, 2001 (Riodinini). This genus was described recently to accommodate four species placed previously in two unrelated genera: Calospila Geyer, 1832 and Chalodeta Stichel, 1910, in the tribes Nymphidiini and Riodinini, respectively (Hall, 2001). Although the taxonomy of Dachetola is apparently clear, no information is available about the biology of these small butterflies.
Dachetola azora (Godart ) (Fig. 1) is the most common species in the genus, which occurs widely throughout south-eastern South America (Hall, 2001). The purpose of this article is to describe some aspects of the natural history and morphology of the last instar larva and pupa of D. azora and provide the first biological information of immature stages for the genus. In addition, the use of mistletoes as host plant in the Riodinidae is reviewed and the morphological and behavioral traits here described are compared with those known for other putatively related genera in Riodinini.
MATERIAL AND METHODS
Collection and rearing of Dachetola azora
In 26 April 2011, two last instar larvae were collected while resting on the stems of a mistletoe Struthanthus sp. (Loranthaceae) (Fig. 1A, B), which was parasitizing a Serjania sp. (Sapindaceae) climber, in the "Reserva Municipal Biologica da Serra do Japi" (~1,100 m a.s.l.) (23[degrees]14'S, 46[degrees]56'W). This area consists of semideciduous, mesophytic forest located in the municipalities of Jundiai and Cabreuva, in Sao Paulo, Southeastern Brazil. The collected larvae were reared in the laboratory in a plastic pot under ambient conditions with food available ad libitum (following Kaminski, 2008). One specimen in last instar stage was fixed in Dietrich fluid. Shed head capsules, pupal exuvia, and the adult are deposited in the Museu de Zoologia "Adao Jose Cardoso" (ZUEC), Universidade Estadual de Campinas, Campinas, Sao Paulo, Brazil.
Measurements were taken and general aspects of morphology were observed using a Leica[R] MZ7.5 stereomicroscope equipped with a micrometric scale. The width of the larval head capsule was measured as the distance between the most external stemmata. The total lengths of larvae and pupae were measured in dorsal view. Color patterns of immature stages in vivo were photographed with a digital camera. Scanning electron microscopy (SEM) was conducted using a JEOL[R] JSM-5800 microscope, with samples prepared according to standard techniques (for details, see Kaminski et al., 2012). The terminology for descriptions of early stages follows Stehr (1987) for general morphology of larvae, Mosher (1916) for pupae, and DeVries (1988) for ant-organs.
Adults of D. azora are found infrequently visiting small flowers as Eupatorium L., Mikania L. (Asteraceae), and Cordia L. (Boraginaceae) (Fig. 1F). A female was observed flying over the host plant where the larvae were found, but oviposition was not observed. Larvae are solitary and remain immobile along the stem of the host plant during the day, leaving at night to feed on the leaves and returning to the same place after feeding. Larvae present cryptic coloration that is similar to mosses and lichens that cover the host plant branch (Fig. 1B, C). The pupa is also cryptic and pupation occurs on the stem of the host plant, where the pupa remains attached to the substrate only by the cremaster, resembling a piece of broken branch (Fig. 1D, E).
Description of immature stages
Last instar (Figs. 1B, C, 2): Duration 15 days (N = 1). Head capsule width 2.32-2.50 mm (N = 2), total length 1.10 cm. Head whitish green; body pale green with some black, gray, and white spots that correspond to microscopic setae, and a brown band dorsally (Fig. 1B, C). Body densely covered with several types of setae (Fig. 2E-G), including dendritic, echinoid, plumose, and perforated cupola organs (PCOs). Conspicuous spatulate-tipped setae are present as follows: at anterior margin on prothoracic shield, in pairs dorsally on other segments (Fig. 2G); directed ventrally in lateral area of thoracic and abdominal segments (Fig. 2F). Prolegs with lateroseries of crochets and several long and apically pointed plumose setae (Fig. 2H). Spiracle on A1 located ventrad and cephalad, whereas that of A2 is aligned with the remaining spiracles and located at center of segment in lateral view.
Pupa (Fig. 1D, E); Duration 16 days (N = 1). Total length 0.90 cm, width at A1 0.23 cm. Body pale green with some brown, black, gray, and white marks. Margin of prothorax ocher with a white spot dorsally on mesothorax, and a conspicuous black spot dorsally on A4 to A5 abdominal segment. Tegument entirely corrugated, with several small tubercles, including basilars on basis of wings, near ocular area, and associated with abdominal spiracles in subspiracular position. Body with several scattered stellate setae, in larger quantities on tubercles. Silk girdle absent. Mesothoracic spiracles black, others brown, with an elevated margin. Consolidated A9 and A10 segments constitute ventrally flat cremaster, which has short crochets in ventral position, and long white plumose setae in margin.
Information about immature stages of Dachetola are described for the first time, and the results are important for better understanding the systematic position of this genus within the Riodinidae.
The placement of D. azora in Riodinini is reinforced by the position of spiracles, presence of echinoid setae, and absence of tentacle nectary organs, which are all typical features of this tribe (Harvey, 1987; Kaminski, 2008). The morphology and behavior of the immature stages suggests a close relationship with Lasaia Bates, 1868 (see DeVries, 1997; and images in Janzen and Hallwachs, 2014); larvae of Lasaia have cryptic coloration while resting on branches, lateral setae directed ventrally, covering the head in front view, and some spatulate-tipped setae laterally and paired dorsally. Similar to Dachetola, the pupa of Lasaia is fixed only by the cremaster without a silk girdle, and looks like a piece of broken branch. Interestingly, Hall (2001) proposed that Dachetola is closely related to Metacharis Butler, 1867 on the basis of male genitalic characters, a relationship that is not evident based on the comparison the immature stages of both genera alone (see Callaghan, 1989, 1991; DeVries, 1997; Janzen and Hallwachs, 2014).
Although represented by only a single record, some behavioral traits observed, such as larval resting on the host branch and the oviposition attempt by the female, provides further evidence that D. azora is a mistletoe specialist, similar to Baeotis Hubner,  spp. (L.L. Mota et al., in prep.). The use of mistletoes (Santalales: Loranthaceae and Viscaceae) by Riodinidae is uncommon, and has been recorded for only eight genera so far (see Table 1). Available records suggest that mistletoe use may be divided in two types: 1) larvae specialists with diets restricted to mistletoes; and, 2) larvae generalists whose diet may include mistletoes, which seems to be the case in Chalodeta chelonis (Hewitson, 1866), which feeds on flower buds, and some myrmecophilous Nymphidiini with polyphagous larvae. In addition to D. azora, other putative mistletoe specialists are Baeotis spp., Cariomothis erythromelas (Sepp, 1841) (Riodinini), and Thisbe hyalina (Butler, 1867) (Nymphidiini). Rhetus Swainson (1829) spp. (Riodinini) is another possible mistletoe specialist. Although some of the above taxa have been reported using several host plant families other than mistletoes (see Beccaloni et al., 2008), recent observations indicate that Rhetus larvae feed on mistletoes (Nishida et al., 2009; Jorge S. S. Bizarro, pers. comm.). Thus, several records from other plant families are probably mistakes, reflecting the observation of larvae and pupae resting on branches of the mistletoe host tree. This type of confusion is quite common in host plant records for mistletoe-feeding butterflies (see DeVries, 1982; Braby and Nishida, 2010).
One of the most striking features in riodinids is the great morphological diversity found in adults (d'Abrera, 1994; DeVries, 1997). Similarly, it is expected that this variety of forms is also reflected in the morphology and ecology of the immatures stages. The present study reveals another small facet of the biology of this amazing group of butterflies.
Caption: Fig. 1. Natural history of Dachetola azora on the mistletoe Struthanlhus sp. A. host plant; B. detail of host plant stem, note the last instar (dashed circle); C. last instar in dorsolateral view; D. pupa in dorsal view; E. pupa in lateral view; F. male visiting flowers of Cordia sp. (Itabirito, Minas Gerais, Brazil).
Caption: Fig. 2. Scanning electron microscopy of last instar of Dachetola azora. A. head in frontal view; B. detail of mouthparts; C. plumose setae near the stemmatal area; D. mesothoracic leg; E. lateral row of setae, note the spatulate-tipped setae (arrow); F. dorsal spatulate-tipped setae; G. spiracle; H. proleg.
We thank Adilson Moreira for help in the field work in the Serra do Japi; Claudenir S. Claires for host plant identification; Eduardo Barbosa for critical reading of the manuscript; Keith Willmott for their helpful comments on the last version of the article. Special thanks to Phil DeVries, Jorge S. S. Bizarro, and Neuza A. Silva for sharing unpublished host plant records. L.A.K. was supported by FAPESP (10/51340-8) and CNPq (163119/2013-9). L.L.M. thanks Pibic/CNPq for a graduate fellowship. A.V.L.F. thanks FAPESP (grant 04/05269-9), and the Brazilian CNPq (fellowship 302585/2011-7). This publication is part of the RedeLep "Rede Nacional de Pesquisa e Conservapao de Lepidopteros" SISBIOTA-Brasil/CNPq (563332/2010-7) and BIOTAFAPESP program (11/50225-3).
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Received 9 March 2014; accepted 23 April 2014
Lucas A. Kaminski (1,2), Luisa L. Mota (1) and Andre V. L. Freitas (1)
(1) Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, CP 6109, 13083-970, Campinas, SP, Brazil
(2) E-mail address for correspondence: firstname.lastname@example.org
Table 1. Summary of host plant records for Riodinidae in mistletoes (Santalales: Loranthaceae and Viscaceae). Riodinidae species Tribe Mistletoe records Localities Baeotis johannae Riodinini Passovia ovata Brazil (DF) Baeotis melanis Riodinini Struthanthus sp. Brazil (SP) Cariomothis Riodinini Viscum verticillatum Suriname erythromelas Chalodeta chelonis Riodinini Passovia ovata Brazil (DF) Dachetola azora Riodinini Struthanthus sp. Brazil (SP) Rhetus arcius Riodinini Struthanthus Costa Rica orbicularis Rhetus periander Riodinini Loranthaceae Brazil (PR) Synargis sp. Nymphidiini Loranthaceae Costa Rica Theope virgilius Nymphidiini Phoradendron Costa Rica quadrangulare Thisbe hyalina Nymphidiini Phoradendron sp. Ecuador Riodinidae species References Baeotis johannae N. P. Silva (pers. comm.) Baeotis melanis L. L. Mota et al. (In prep.) Cariomothis Sepp (1840) erythromelas Chalodeta chelonis N. P. Silva (pers. comm.) Dachetola azora Present study Rhetus arcius Nishida et al. (2009) Rhetus periander J. M. S. Bizarro (pers. comm.), Beccaloni et al. (2008) Synargis sp. DeVries (1997) Theope virgilius Janzen and Hallwachs (2014) Thisbe hyalina DeVries (1997) Brazilian state abbreviations: DF, Distrito Federal; PR, Parana; SP, Sao Paulo
Please note: Illustration(s) are not available due to copyright restrictions.
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|Author:||Kaminski, Lucas A.; Mota, Luisa L.; Freitas, Andre V.L.|
|Date:||Jan 1, 2014|
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