BIOLOGIJA. 2017. Vol. 63. No. 3. P. 230–237 © Lietuvos mokslų akademija, 2017

Anacardiaceae-feeding Nepticulidae in the Neotropics: description of Stigmella lilliputica sp. nov. from Argentina, a pest on Chilean peppertree polygama

Jonas Rimantas Stonis1*, The paper deals with a description of a new leaf-mining Nept- iculidae species, Stigmella lilliputica Remeikis & Stonis, sp. nov., Andrius Remeikis2 from Argentina, the larvae of which feed on leaves of the Chilean peppertree Schinus polygama (Cav.) Cabrera. The species is illus- 1 Lithuanian University of Educational trated with photographs of the adults and leaf mines, a distribu- Sciences and Baltic-American tion map as well as drawings and photographs of the genitalia. Biotaxonomy Institute, Studentų St. 39, Vilnius 08106, Lithuania Keywords: , leaf mines, Nepticulidae, new species, Schinus L. 2 Institute of Ecology, Nature Research Centre, Akademijos St. 2, Vilnius 08412, Lithuania

INTRODUCTION the preliminary analysis by Remeikis et al. (2016), the Nepticulidae feeding on Asteraceae , The family Nepticulidae (pygmy moths) has been in contrast to the Holarctic fauna, were recorded characterized in monographic reviews by Johans- for some 24% of the trophically investigated taxa; son et al. (1990) and Puplesis (1994) and, with on Rosaceae, for about 15%; on Lamiaceae, 13%; special reference to South America, by Puplesis, on Fagaceae, 9%; on Euphorbiaceae, 5%; on Fa- Robinson (2000) and Stonis et al. (2016). baceae and Malvaceae, about 4% (each); on Ur- Larvae of pygmy moths mine during all instars, ticaceae, 3%; on Polygonaceae, Melostomataceae, feed inside leaves, and occasionally other green and Ericaceae, 2.5% (each); and on Grossulari- tissues of plants. The vast majority of the species aceae, Salicaceae, Rhamnaceae, Myrtaceae, Scro- are monophagous or strictly oligophagous. There- phularia ceae, and Verbenaceae, nearly 2% (each). fore, studies of feeding preferences of these spe- Some Nepticulidae were also found on Gunner- cialized leaf-mining insects are a priority goal. aceae, Geraniaceae, Meliaceae, Rubiaceae, and As regards the Neotropical species, exten- Boraginaceae (almost 1% each) (Remeikis et al., sive studies of their trophic relationships started 2016). There are also species trophically associ- only recently. It is known that a vast majority of ated with Anacardiaceae (though very few). It the Neotropical Nepticulidae are trophically asso- should be noted that the percentages counted by ciated with either Asterids or . As a result of Remeikis et al. (2016) include only two (not three) Anacardiaceae-feeding species out of the currently * Corresponding author. Email: [email protected] known three species listed in Fig. 1. The host- Anacardiaceae-feeding Nepticulidae 231 family Anacardiaceae (the sumac family) com- Institutional abbreviation used in the text: prises about 78 genera and more than 700 spe- ZMUC – Zoological Museum, University of cies of evergreen or deciduous trees, shrubs, Copenhagen. and woody vines (Mitchell, 2004). The family is native to tropical and subtropical areas, with RESULTS several species occurring in temperate regions. The primary centres of diversity are in Mexico, Stigmella lilliputica Remeikis & Stonis, South America, southern and equatorial Afri- sp. nov. ca, and South East Asia (Mitchell, 2004). Type material. Holotype: ♂, ARGENTINA, During the course of the present study, we Rio Negro, 50 km E of Choele Choel, caught examined large samples of reared Nepticuli- around Schinus polygama (Cav.) Cabrera, dae material from Central and South America, elevation ca. 170 m, 13.ix.1981, E. S. Niels- including some material collected by Danish en & O. Karsholt, genitalia slide no. RA584♂ entomologists in 1981 in the biogeographi- (ZMUC). Paratypes: 5 ♂, 2 ♀, same label cal province of Monte (Argentina). Our study data, genitalia slide nos. RA585♀, RA588♂, revealed one species associated with the host RA631♂, RA632♂ (ZMUC). Additional exam- plant from the Anacardiaceae family (which is ined material: a collection of leaf-mine samples, described in the current paper). same label as paratypes (ZMUC). Diagnosis. In the male genitalia, the combi- MATERIALS AND METHODS nation of a small U-shaped gnathos, very long apical process of valva, and a pair of spine-like The description of the new species is based on cornuti distinguishes S. lilliputica sp. nov. from material deposited in the collection of the Zoo- all other Stigmella. The host plant (Schinus po- logical Museum, Natural History Museum of lygama) also makes this species distinctive. Denmark in Copenhagen, Denmark, which was Male (Fig. 2). Forewing length about 1.8 mm; collected in Argentina in 1981 by E. S. Nielsen wingspan about 4.1 mm. Head: palpi and face and Ole Karsholt during the international expe- almost white; frontal tuft dark grey-brown on dition Mision Cientifica Danesa. Collecting me- vertex, pale orange to cream white on frons; col- thods and protocols for species identification and lar brownish cream; scape white, glossy; antenna description are outlined in Puplesis, Robinson longer than half the length of forewing; flagel- (2000) and Stonis et al. (2016). After maceration lum with about 39 segments, grey to dark grey. of the abdomen in 10% KOH and subsequent Thorax and tegula grey, with some fuscous scales cleaning, male genital capsules were removed anteriorly; forewing grey, at certain angle some from the abdomen and mounted ventral side up- scales grey-white or cream white tipped; fascia permost. The phallus was removed and mounted of forewing postmedian, wide, comprised of in Euparal separately but on the same genitalia grey-white, non-shining scales; the narrow area slide. Abdominal pelts and female genitalia were before fringe and forewing’s apex black-brown; stained with Chlorazol Black (Direct Black 38/ fringe grey to almost white; underside of fore- Azo Black) (for a detailed description of the me- wing grey-brown, without spots. Hindwing grey thod, see Stonis et al., 2014). to pale grey on upper side and underside, with- Permanent slides were photographed and out spots or androconia; fringe grey. Legs cream studied using a Leica DM2500 microscope grey, with fuscous scales on upper side. Abdo- and Leica DFC420 digital camera. The descrip- men black-grey on upper side, dark grey on un- tive terminology of morphological structures derside; genital segments grey; anal tufts short, follows Puplesis, Robinson (2000), except for indistinctive, dark grey. the term “aedeagus”, which is referred here as Female (Fig. 3). Forewing length 1.6–1.7 mm; “phallus”, and the term “cilia”, which is referred wingspan 3.9–4.0 mm. Antenna shorter than half here as “fringe”. the length of forewing, usually curved (number 232 Jonas Rimantas Stonis, Andrius Remeikis

Fig. 1. Leaf mines of Stigmella lilliputica Remeikis & Stonis, sp. nov. on Schinus polygama, Mon- te province, Argentina (* possibly the initial gallery starts in a leaf vein) Anacardiaceae-feeding Nepticulidae 233

Figs. 2–9. Stigmella lilliputica Remeikis & Stonis, sp. nov. 2 – male adult, holotype; 3 – female adult, para- type; 4 – male genitalia, dorsal view of capsule, slide no. RA584, holotype; 5, 6 – same, uncus and gnathos, genitalia slide no. RA588, paratype; 7 – same, phallus, genitalia slide no. RA588, paratype; 8 – same, slide no. RA584, holotype; 9 – same, ventral view of capsule, slide no. RA588, paratype (ZMUC) 234 Jonas Rimantas Stonis, Andrius Remeikis of segments unknown). At certain angle of view, Male genitalia (Figs. 4–15). Capsule longer base of forewing with distinctly cream-tipped (190–205 μm) than wide (115–125 μm). Un- scales. Abdomen dark grey on upper side, grey cus (Figs. 4, 5, 13, 14) thickened only laterally. cream on underside. Otherwise as in male. Gnathos very small (Figs. 11, 12), U-shaped

Figs. 10–16. Genitalia of Stigmella lilliputica Remeikis & Stonis, sp. nov. 10 – male geni- talia, ventral view of capsule, slide no. RA588, paratype; 11, 12 – same, slide no. RA584, holotype; 13 – same, uncus and gnathos, slide no. RA584, holotype; 14 – same, slide no. RA588, paratype; 15 – same, cornuti, slide no. RA584, holotype; 16 – female genitalia, slide no. RA585 (ZMUC) Anacardiaceae-feeding Nepticulidae 235

(Figs. 4, 6). Valva (Fig. 9) 140–150 μm long, South American species, Stigmella schinivora, 35–40 μm wide, with very large apical process was described and illustrated by the Dutch re- (Fig. 11, 12); transtilla (Figs. 4, 11) with trian- searcher E. J. van Nieukerken (van Nieu- gular sublateral processes. Vinculum with shal- kerken et al., 2016) on the basis of his mate- low anterior excavation and weakly developed rial collected in August 2000 in Cataratas del lateral lobes. Phallus (Figs. 7, 8) 145–150 μm Iguazú, Argentina. The third species,Acalyptris long, 60 μm wide; vesica with two 30 μm long yucatani Remeikis & Stonis was described and spine-like cornuti (Fig. 15). illustrated from a single female specimen col- Female genitalia (Fig. 16). Total length lected in Central America, the Yucatán pen- about 440 μm. Abdominal apex wide, distinct- insula province (Stonis et al., 2013) (Fig. 1). ly truncate. Anterior and posterior apophyses The host plants of all three currently known slender. Vestibulum relatively wide, without Nepticulidae species feeding on Anacardiaceae sclerites. Accessory sac indistinctive. Ductus belong to a single (Schinus L.). The plants spermathecae probably broken (missing) in of this genus are well represented in the flora Fig. 16. Corpus bursae oval-shaped, 235 μm of the Neotropics and are commonly known long, 190 μm wide; pectinations indistinctive or as peppertrees; it is the only genus occurring absent (not visible in slide no. RA585; Fig. 16). naturally above 3,000 meters (Mitchell, 2004). Bionomics (Fig. 1). Host plant: Schinus po- Some species of Schinus may become invasive lygama (Cav.) Cabrera (Anacardiaceae). Judg- outside their natural habitats. Schinus polyga- ing from the collected empty leaf mines, larva ma, a newly recorded host plant of Stigmella lil- mines in leaf of Chilean peppertree in August. liputica sp. nov., is an expanding invasive plant Egg on upper side or underside of the leaf blade, outside its natural range, e.g., in California, usually on mid vein, sometimes on lateral vein USA (The Global Invasive Species Team, 2009). of the leaf. Leaf mine (Fig. 1) as a sinuous or In tropical America, there are about 33 genera contorted gallery with a line of black frass; frass and 170 species of Anacardiaceae plants, includ- fills about 2/3 of the width of the gallery. It is ing the largest genus, Rhus, with 25 species solely supposed that the gallery starts inside the leaf from tropical America (Mitchell, 2004). Rhus, vein. Larval exit slit on upper side of the leaf. along with few other Anacardiaceae genera, such Adults fly in September. as Pistacia, Cotinus, etc., has been confirmed as Distribution (Figs. 1). This species occurs a host plant for few Nepticulidae species in bo- in Argentina (Monte biogeographical province real regions (see the Catalogue of Nepticuloidea of South American transition zone) at altitudes by Diškus, Puplesis, 2003). At least two species about 170 m. of Rhus-feeding Stigmella (Nepticulidae) are de- Etymology. The species is named after Lilli- scribed from Nearctic America (Newton, Wilkin- putians, miniature people from Gulliver’s Travels son, 1982); in total, the fauna of the Nearctics and by Jonathan Swift in reference to the small size of Palaearctics counts at least six Anacardiaceae- the adults and particularly because of the unusu- feeding species (Diškus, Puplesis, 2003). ally miniature gnathos in the male genitalia. Drawing on the great diversity of potential Remarks. The host plantSchinus polygama Anacardiaceae host plants in tropical and sub- (the Chilean peppertree or Hardee peppertree) tropical America, we suppose that the Anacardi- is native to Argentina and Chile and natural- aceae-feeding Nepticulidae fauna is much richer ized (invasive) in California. than is presently known. So far, in the Neotrop- ics, the Nepticulidae trophically associated with DISCUSSION Anacardiaceae account for about 1% of the cur- rently described and pending for description Currently three species of Anacardiaceae-feed- trophically investigated taxa (including our own ing Nepticulidae are known from the Neotrop- field records of purely leaf mines without reared ics. Along with our Stigmella lilliputica, another adults). 236 Jonas Rimantas Stonis, Andrius Remeikis

It is interesting to note that recent surveys in 5. Newton PJ, Wilkinson C. A taxonomic revi- southern Florida, USA, Brazil, and Argentina sion of the North American species of Stig- carried out with the purpose of assisting biologi- mella (Lepidoptera: Nepticulidae). System En- cal control agents to deal with the invasive Bra- tomol. 1982; 7(4): 367–463. zilian peppertree Schinus terebinthifolius have 6. Puplesis R. The Nepticulidae of Eastern Eu- revealed four previously unknown species and rope and Asia: western, central and eastern one new genus of another Lepidopteran family parts. Leiden: Backhuys Publishers; 1994. of leaf miners, Gracillariidae (Davis et al., 2011). 291 p. 7. Puplesis R, Robinson GS. A review of ACKNOWLEDGEMENTS the Central and South American Nepticu- lidae (Lepidoptera) with special reference The authors are indebted to Ole Karsholt and to Belize. Bull Nat Hist Mus Entomol. 2000; the late Professor N. P. Kristensen (ZMUC) 69(1): 3–114. for the initial stimulus to start the Neotropical project together with generous support during 8. Remeikis A, Diškus A, Stonis JR. Prelimi- its course as well as the loan of the Neotropi- nary trophic analysis of leaf-mining Nept- cal material. This study was partially supported iculidae: pronounced feeding strategies in by the Research Foundation of the Lithuanian Middle and South America? Biologija. 2016; University of Educational Sciences (2017). 62(4): 207–14. 9. Stonis JR, Diškus A, Remeikis A, Gerulaitis V, Received 11 August 2017 Karsholt O. Leaf-mining Nepticulidae (Lepi- Accepted 13 September 2017 doptera) from record high altitudes: docu- menting an entire new fauna in the Andean páramo and puna. Monograph. Zootaxa. References 2016; 4181(1): 1–94. 10. Stonis JR, Diškus A, Remeikis A, Navickaitė A. 1. Davis DR, Mckay F, Oleiro M, Vitorino MD, Study methods of Nepticulidae: micro-mounts Wheeler GS. Biology and systematics of of genitalia structures. In: Stonis JR, Hill SR, the leafmining Gracillariidae of Brazilian pep- Diškus A, Auškalnis T, editors. Selected ab- per tree, Schinus terebinthifolius Raddi, with stracts and papers of the First Baltic Interna- descriptions of a new genus and four new spe- tional Conference on Field Entomology and cies. J Lepid Soc. 2011; 65(2): 61–93. Faunistics. Vilnius: Edukologija Publishers; 2. Diškus A, Puplesis R. Catalogue of the world 2014. p. 32–35. Nepticuloidea & Tischerioidea. In: Puplesis R, 11. Stonis JR, Remeikis A, Diškus A, Noreika R. Diškus A, editors. The Nepticuloidea & Tisch- New Nepticulidae species (Insecta, Lepidop- erioidea (Lepidoptera) – a global review, with tera) from the Yucatán Peninsula (SE Mexico). strategic regional revisions. Lututė Publishers, Zootaxa. 2013; 3609(2): 223–30. Kaunas, 2003; p. 18–436. 12. The Global Invasive Species Team. Schinus 3. Johansson R, Nielsen ES, van Nieukerken EJ, polygamus (Cav.) Cabrera (Peruvian pep- Gustafsson B. The Nepticulidae and Oposte- pertree). https://www.invasive.org/gist/alert/ gidae (Lepidoptera) of North West Europe. alrtschi.html. Updated March 2009. Retrieved Fauna Entomol Scand. 1990; 23(1/2): 1–739. 29 July 2017. 4. Mitchell JD. Anacardiaceae. In: Smith N, 13. Van Nieukerken EJ, Doorenweerd C, Nishi- Mori SA, Henderson A, Stevenson DWm, da K, Snyers C. New taxa, including three new Heald SV, editors. Flowering plants of the Ne- genera, show uniqueness of Neotropical Nep- otropics. Oxford, Princeton University Press. ticulidae (Lepidoptera). ZooKeys. 2016; 628: 2004; 594 p. 1–63. Anacardiaceae-feeding Nepticulidae 237

Jonas Rimantas Stonis, Andrius Remeikis

PIETŲ AMERIKOS MAŽIEJI GAUBTAGAL- VIAI (NEPTICULIDAE), TROFIŠKAI SUSIJĘ SU ANACARDIACEAE: NAUJOS RŪŠIES STIGMELLA LILLIPUTICA, MINUOJANČIOS SCHINUS POLYGAMA LAPUS, APRAŠYMAS

Santrauka Straipsnyje pateikti naujausi Pietų Amerikos Anacardiaceae augalus minuojančių mažųjų gaub- tagalvių (Nepticulidae) tyrimų rezultatai ir aprašo- ma viena nauja mokslui rūšis – Stigmella lilliputica Remeikis & Stonis, sp. nov. Ši Argentinoje aptinka- ma rūšis pasižymi išskirtine genitalinių struktūrų morfologija ir yra plintančio invazinio Schinus po- lygama (Cav.) Cabrera minuotoja. Iš viso šiuo metu registruotos trys mažųjų gaubtagalvių rūšys, kurios Vidurio ir Pietų Amerikoje minuoja Anacardiacae augalus. Raktažodžiai: Anacardiaceae, lapų minuotojai, mažieji gaubtagalviai, naujos rūšys, Nepticulidae, Schinus L.