Cotinus Obovatus) Author(S): Donald R

A New Leafmining Moth (Cameraria cotinivora, Lepidoptera: Gracillariidae) of the American Smoketree (Cotinus obovatus) Author(s): Donald R. Davis and Gary R. Graves Source: Proceedings of the Entomological Society of Washington, 118(2):244-253. Published By: Entomological Society of Washington DOI: http://dx.doi.org/10.4289/0013-8797.118.2.244 URL: http://www.bioone.org/doi/full/10.4289/0013-8797.118.2.244

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A NEW LEAFMINING MOTH (CAMERARIA COTINIVORA, LEPIDOPTERA: GRACILLARIIDAE) OF THE AMERICAN SMOKETREE (COTINUS OBOVATUS)

DONALD R. DAVIS AND GARY R. GRAVES

urn:lsid:zoobank.org:pub:AC9C2C2D-D999-463E-8599-8185C62D94F3

(DRD) Department of Entomology, National Museum of Natural History, Smithsonian Institution, P.O.Box 37012, MRC 168, Washington, D.C. 20013-7012, USA, urn:lsid:zoobank.org:author:4DE643F9-237B-4330-99FB-44B7159FF9C4 (e-mail [email protected]); (GRG) Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, P.O.Box 37012, MRC 116, Washington, D.C. 20013-7012, USA, and Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, DK-2100, Copenhagen Ø, Denmark, urn:lsid:zoobank.org:author:565707D4- E032-4CDF-96D0-91CED9FF1EC9 (e-mail [email protected])

Abstract.—Fieldwork in the Ozark Mountains of the central United States by GRG over the last decade involving the American smoketree, Cotinus obovatus Raf. (Anacardiaceae), has resulted in the discovery of a previously unknown moth species belonging to the genus Cameraria (Lepidoptera: Gracillariidae). The larva of this species mines the leaf mesophyll of this tree, creating serpentine mines most visible from the upper (adaxial) surface of the leaf. The most closely related species to Cameraria cotinivora,n.sp.isCameraria guttiﬁnitella (Clemens), a common leaf- minerofpoisonivy,Toxicodendron radicans (L.) Kuntze (Anacardiaceae). Illustrations of both species are provided as well as a COI analysis of their genetic relationship. Key Words: American smoketree, Cameraria cotinivora, Cameraria guttiﬁnitella, Cotinus obovatus, Gracillariidae, leafminer, taxonomy DOI: 10.4289/0013-8797.118.2.244

With the discovery of C. cotinivora, reddish to orange brown forewings, of- the predominantly Nearctic genus Cam- ten with 2-3 white fasciae with external eraria currently includes 54 species margins bordered by black scales. The known to range over most of North eighth abdominal sternite of the male is America and southern Canada, with enlarged and highly modiﬁed, usually several species yet to be described. extending part way beneath the genitalia, Fewer than 30 species have been re- as often in the genus Phyllonorycter. ported from the Old World, i.e., the American smoketree (Cotinus obova- Oriental, Palearctic, and Afrotropical tus Raf., Anacardiaceae, Fig. 8) is a rare regions(DePrins&DePrins2015).Adult North American shrub or small tree Cameraria are usually characterized by known from three disjunct populations VOLUME 118, NUMBER 2 245

(Fig. 1) in south-central Texas, on the The European smoketree is chemi- Ozark Plateau in Arkansas, Missouri, cally protected (Fraternale & Ricci and Oklahoma, and from the southern 2014) and the same is likely true for the Cumberland Plateau in northeastern poorly studied but closely related Alabama and adjacent Tennessee and American smoketree (Miller et al. 2001). Georgia (Little 1977). Few specimens The only recorded native herbivore of have trunk diameters exceeding 30 cm or the American smoketree is a notodontid have canopy heights greater than 12 m moth, Datana perspicua Grote and (mature trees usually range between Robinson (Crocker & Simpson 1982). 4-6 m in height). The simple ovate Documentation of native communities leaves (8-15 cm) have entire margins of phytophagous insects that feed on the and long petioles. The plants are usually American smoketree is of particular in- dioecious with small flowers in loose terest given the tree’s rarity and its panicles that appear in April and May. fragmented natural geographic range. Flower pedicels elongate after flowering, The proposed introduction of biocontrol and those on abortive flowers become agents to counter the invasive Brazilian plumose which lends a smoky appear- pepper-tree (Schinus terebinthifolia Raddi, ance to the tree when viewed from Anacardiaceae) in Florida (Medal et al. a distance. The dark yellow wood was 1999, Manrique et al. 2008) may pose used sporadically in the 19th century as a conservation risk to the distantly re- a source of fustic dye and for fence posts lated American Smoketree. Thus there owing to its resistance to decay. All is an urgent need for immediate taxo- known populations occur on soils de- nomic identification of all native and rived from calcareous bedrock, typically introduced herbivores of the American in glades and on cliffs and bluffs. They Smoketree. occur less frequently in mixed hardwood- GRG first encountered gracillariid cedar woodland. American smoketree leaf mines in populations of the Ameri- is only occasionally cultivated as an can smoketree on the Ozark Plateau ornamental, as most gardeners prefer its while mapping the geographic distribu- showier relative, the European smoke- tion of the host. Here we report that this tree (Cotinus coggygria Scop.), which leafminer represents a new species of ranges from southern Europe eastward Cameraria (Lepidoptera: Gracillar- across central Asia to northern China. iidae), most closely related to Cameraria For more than a decade GRG has been guttifinitella, a common leafminer of engaged in a general survey of Cotinus poison ivy, Anacardiaceae, Toxicoden- obovatus in order to better define its geo- dron radicans (L.) Kuntze. Cameraria graphic range and to collect genetic sam- guttifinitella has also been reared from ples from populations on the Ozark Plateau Rhus aromatica Aiton in Canada by and on the southern Cumberland Plateau. It T. N. Freeman and E. van Nieukerken. was also suspected that the relative rarity and the highly fragmented geographic range of the plant might reveal some in- MATERIALS AND METHODS teresting relationships among the insect Specimens examined in this study are herbivores. Thus far only specimens of C. deposited in the former United States Na- cotinivora have been found mining the tional Museum (USNM), now the National leaves, but some disjunct populations of the Museum of Natural History, Smithsonian plant have not been examined thoroughly. Institution, Washington, D.C., USA. 246 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Fig. 1. Distribution of Cotinus obovatus (light gray) and of Cameraria cotinivora (dark gray).

Specimen preparation: Genitalic dis- (Oiagen, Inc., Valencia, CA), or from sections were cleared by heating in hot abdomens and larvae using the pro- 10% KOH for ; 30 minutes, and sub- cedures discussed in Nieulerken et al. sequently cleaned and stained with 2012. Primers LepF1 and LepR1 (Hebert either 2% chlorazol black E or mercu- et al. 2004), or the list of primers shown rochrome solutions. Genitalic illustra- in Table 1 of Nieulerken et al, 2012, tions were drawn from dissections were used to obtain the barcoding frag- temporarily stored in glycerine, which ment of COI following methods pre- were later permanently embedded in viously described (Hajibabaei et al. Canada balsam. Genitalic terminology 2006, Nieulerken et al. 2012). Sequences follows Klots (1970) and Kristensen are available in GenBank (http://www. (2003). Sequences of the 658bp mito- nchi.nlm.nih.gov/genbank/) and BOLD chrondrial cytochrome oxidase subunit I (http://www.boldsystems.org/index.php/) gene (CO1) were generated at the Bio- databases. A neighbor-joining (NJ) tree diversity Institute of Ontario, University was generated from nucleotide sequences of Guelph, Canada and the Naturalis using the BOLD aligner as implemented Biodiversity Center, Leiden, the Neth- in BOLD (Ratnasingham and Hebert, erlands. DNA was extracted from legs 2007, 2013). Phylogenetic and molecular using a QIAGEN DNeasy Extraction Kit evolutionary analyses were conducted VOLUME 118, NUMBER 2 247

Table 1. Sample information for specimens submitted for COI barcoding. Additional specimen data as well as sequence data are available on the BOLD website at RDOPO Basal Lepidoptera.

GenBank Species of Accession Sample ID Cameraria Locality BOLD Process ID Number

USNMENT00656313 cotinivora USA: Missouri; Ozark MNAM083-10 JF858636 County, County Road 514 USNMENT00656311 cotinivora USA: Arkansas; Newton MNAM081-10 KU380344 County, Erbie Campground Road USNMENT00656308 cotinivora USA: Arkansas; Newton MNAM078-10 JF858633 County, Erbie Campground Road USA: Arkansas USNMENT00656312 cotinivora USA: Arkansas; Newton MNAM082-10 JF858635 County, Erbie Campground Road USA: Arkansas USNMENT00656309 cotinivora USA: Arkansas: Baxter MNAM079-10 JF858634 County, Denton Ferry Road BIOUG01927-C03 guttifinitella USA: Arkansas; Perry County, BBLOE920-12 KU380340 Toad Suck Ferry Park RMNH.INS.552280 guttifinitella USA: North Carolina: Haywood WOGRA022-13 KU380343 County; Great Smoky Mountains National Park DNA-ATBI-5043 guttifinitella USA: Tennessee, Blount County LGSME043-06 KU380341 CLV291011 guttifinitella USA: Washington D.C. GRPAL657-11 KU380339 RMNH.INS.552279 guttifinitella USA: North Carolina WOGRA021-13 KU380345 RMNH.INS.30477 guttifinitella USA: Virginia WOGRA130-15 KU380342

using MEGA version 6 (Tamura et al. black scales, a pattern (Figs. 2–3) similar 2013). in several species of North American Cameraria. The subapical fascia, al- RESULTS though incomplete, is more preserved in Cameraria cotinivora Davis and C. guttifinitella (Fig. 3) and the apical Graves, new species white spot is more distinct than in C. cotinivora (Fig. 2). The valva of the male Figs. 1–2, Figs. 4, Figs. 6, Figs. 9–11 genitalia of C. cotinivora (Fig. 4a) differs urn:lsid:zoobank.org:act:0284DAD6- from that of guttifinitella (Fig. 5a) in the 4E14-4106-9AC9-EA3BCF3D99BB sacculus being less pronounced (less con- Diagnoses.—Cameraria cotinivora is stricted distally). The saccus of cotinivora most similar, both morphologically and is also more truncate, the base of the genetically, to Cameraria guttifinitella phallus is more swollen, and the vincular (Figs. 3, 5, 7), a common leafminer of process and anellus are more slender than another North American member of the in guttifinitella. In the female genitalia both plant family Anacardiaceae, Toxicoden- the anterior and posterior apophyses are dron radicans. They are the only known relatively shorter in cotinivora (Fig. 6a) North American Cameraria known to feed than in guttifinitella Fig. 7a), and the cau- on Anacardiaceae. The forewings of both dal margin of the eighth sternite is less species possess a pair of prominent white sclerotized in cotinivora. A neighbor- fasciae that are bordered externally by joiningtreeofthegeneticdistancesfor 248 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Figs. 2–3. Adults. Scale = 2 mm. 2. Cameraria cotinivora. Holotype ♂.3.Cameraria guttiﬁnitella ♀, Piscataway National Park, Prince Georges County, Maryland. cytochrome c oxidase I (COI) computed smooth, with broad, silvery white scales; by the Biodiversity Institute of Ontario, vertex rough, with long, white piliform University of Guelph, Canada for Cam- scales partially intermixed below with eraria cotinivora and C. guttiﬁnitella re- similar light reddish brown, piliform vealed a divergence of ; 4% (Fig. 12). scales; scales of vertex directed some- Description.—Adult (Fig. 2). Fore- what forward as a pair of short, lateral wing length 2.4–3.0 mm. Head: Frons tufts; a faint band of reddish brown VOLUME 118, NUMBER 2 249

Figs. 4–7. Genitalia. Scale = 0.2 mm. 4. Male, Cameraria cotinivora. 4a. Ventral view, USNM slide 33848. 4b. Eighth sternite, ventral view. 4c. Phallus, lateral view. 5. Male, Cameraria guttiﬁnitella. 5a. Ventral view, USNM slides 17071, 17076. 5b. Eighth sternite, ventral view. 5c. Phallus, lateral view. Figs. 6 – 7. Female, 6. Cameraria cotinivora. 6a. Lateral view USNM slide 33850. 6b. Ventral view. 7. Female, 7. Cameraria guttiﬁnitella. 7a. Lateral view, USNM slide 18306. 7b. Ventral view. 250 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Figs. 8–11. 8. Cotinus obovatus Raf. Tulsa County, Oklahoma. 9 - 11. Leafmines of Cameraria cotinivora on Cotinus obovatus. Baxter County, Arkansas, (photographed 29 July 2006). piliform scales extending above frons be- with white bases; subapical fascia poorly tween antennal bases. Antenna ; 0.83x developed, with only a portion near dor- the length of forewing; ﬂagellomeres sal edge of wing evident; black tipped smoothly scaled, white ventrally, dark scales around apex of wing with broad, fuscous dorsally with paler scale bases. pale brownish bases that form a subapical Labial palpus straight, directed ventrad, band around wing tip; fringe yellowish and covered with silvery white, smooth white around apex of wing, pale grayish scales; apical segment with a few black white and longer along dorsal margin. scales. Thorax: Pronotum and tegula light Hindwing uniformly light gray. Foreleg reddish brown with a pair of relatively mostly black dorsally and white ven- broad bands of white scales diverging trally; tarsomeres with two white annuli; from head caudally across tips of tegulae. midleg mostly white with dorsal black Venter of thorax mostly white. Forewing spot at base of femur, three dorsal black mostly light reddish brown with two spots on tibia and two dorsal black areas slender, prominent, slightly curved, white on tarsus; hindleg mostly white with two fascia extending diagonally across basal small black spots on femur; apical half of third and just beyond middle of wing; tibia mostly dark brown to fuscous and outer margins of fasciae bordered with tarsus with two black annuli. Abdomen: black scales; subapical region of forewing Brownish fuscous dorsally and laterally, complex, mostly covered by black scales white ventrally. Eighth sternite of male VOLUME 118, NUMBER 2 251

Fig. 12. Neighbor-joining tree of genetic distances (K2P model) for cytochrome c oxidase I (COI) for Cameraria cotinivora and Cameraria guttiﬁnitella. End-branch labels are specimen Sample IDs, followed by the sequence length, and geographic origin.

(Fig. 4c) generally triangular, approxi- Larval mines (Figs. 9 - 11): The mately as long as broad when ﬂattened. feeding by the larvae of Cameraria co- Male genitalia (Figs. 4a–c): Tegumen tinivora create serpentine mines most moderately elongate, ; 0.7x length visible from the upper (adaxial) surface of valva, triangular with semi-acute, taper- of the leaf. The early subepidermal ing apex. Valva elongate, slender with sapfeeding mine is usually obliterated by evenly rounded apex; a slight, smoothly the later broader, full depth serpentine curved constriction present immediately mine. The latter mines are moderately distad of sacculus. Vinculum-saccus shorter broadly tubular and are of approximately than eighth sternite, with mostly truncate similar width throughout most of their anterior apex; caudal medial extension of length. Pupation occurs in a loose cocoon vinculum (vincular process) long and at the distal, sometimes slightly enlarged, slender, ; 0.5x the length of valva. Phallus rounded, terminal end of the mine. slender, ; equal to length of valva, and HOLOTYPE: UNITED STATES: with swollen base ; 4.5x width of phallus ARKANSAS: Baxter Co: Denton Ferry Rd: at midlength. Female genitalia (Figs. 36⁰21.00’N, 92⁰31.79’W: ♂, 29 Jun 6a-b): Anterior apophysis ; 0.83x length 2008, Gary R. Graves; Host: DRD 2685, of posterior apophysis. Ostium a simple, Cotinus obovatus Raf,; Digital image, slightly enlarged opening at caudal edge (USNM holotype 01066895). of eighth sternum. Ductus bursae elon- PARATYPES: Described from a total gate, ; 4.3x length of posterior apoph- of 16♂ and 26♀. UNITED STATES: ysis, gradually enlarging to ; spherical ARKANSAS: Baxter Co: Denton Ferry Rd: corpus bursae; signum absent; duct of 36⁰21.00’N, 92⁰31.79’W: 4♂,6♀,29Jun accessory bursae arising near caudal end 2008, em. 4-14 Jul 2008, Host: DRD of ductus bursae just before ostium. 2681, Cotinus obovatus Raf., 2♂,1♀, Host: Anacardiaceae: Cotinus obova- em. 16-24 Jul 2008; 1♀, em. 4-14 Jul, tus Raﬁnesque (American smoketree). BOLD DNA 00656311; 1♀, em. 15 Jul 252 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

2008, BOLD DNA 00656312; 2♀,em. Darrow of the Department of Entomology, 16-24 Jul, BOLD DNA 00656309, Smithsonian Institution, for the illustra- 00656310; 36⁰21.22’N, 92⁰31.61’W: 2♂, tions, graphics, and the preparation of 3♀, em. 15 Jul 2008; 1♀, 4-9 Jul 2008; plates used in this publication. Donald Marion Co: Marion County Road 7033: Harvey and Margaret Rosati also assisted 36⁰15.139N, 92⁰32.429W: 1♂, 4 Jul 2007, in preparing the neighbor-joining tree Host: DRD 2668, Cotinus obovatus Raf., (ﬁgure 12). We especially thank Margaret em. 7 Jul 2007, USNM slide 33848; Host: Rosati, Department of Entomology, DRD 2668: Cotinus obovatus Raf, 1♀, Smithsonian Institution, for her assistance em. 7 Jul 2007, USNM slide 33850; 2♀, in assembling the barcode tree data. We em. 10 Jul 2007, 1♀, em. 22 Jul 2007, thank Jean F. Landry, Agriculture Canada, Host: DRD 2669: Cotinus obovatus Raf,, Camiel Doorenweerd and Erik van 1♀, em. 12 Jul 2007; Host: DRD Nieukerken, Naturalis Biodiversity Cen- 2670: Cotinus obovatus Raf,, 1♂,em.19 ter, Leiden, The Netherlands , and Carlos Jul 2007, Gary R. Graves; Newton Co; Lopez-Vaamonde, INRA Orle´ans, Unite´ Erbie Campground Rd, 36⁰ 04.19’N, de Recherche en Zoologie Forestie`re, 93⁰12.65’W, 26 Jun 2008, Host: DRD France for their permission to use their 2682: Cotinus obovatus Raf, 1♂,8-10Jul barcode data, and to Paul Hebert and 2008; 1♂,1♀, em. 10 Jul 2008; Host Jeremy deWaard of the Biodiversity In- DRD: 2681: 1♀, 16-24 Jul 2008, BOLD stitute of Ontario, University of Guelph, DNA 00656308, Gary R. Graves. MIS- Canada, for providing barcode data. Fi- SOURI: Ozark Co: Ozark County Road nancial support for DNA barcoding was 514: 36⁰32.12’N, 92⁰26.18’W: 1♂,23 provided by the government of Canada Jun 2007, em.19 Jul 2007, Host DRD : through Genome Canada and the Ontario Cotinus obovatus Raf, 29 Jun 2008, Host: Genomics Institute in support of the In- DRD 2684: Cotinus obovatus Raf, 1♀, ternational Barcode of Life project. Mi- em. 15 Jul 2008, BOLD DNA 00656313, gnon Davis assisted with data capture and Gary R. Graves; 36⁰31.99’N, 92⁰25.88’W: specimen curation. GRG was supported 29 Jun 2008, Host: DRD 2683: Cotinus by the Alexander Wetmore Fund, Smith- obovatus Raf, 1♂,1♀, em. 4-10 Jul 2008; sonian Institution, and by the Smoketree 36⁰32.12’N, 92⁰26.18’W: 29 Jun 2008, Trust. Finally we thank Erik van Nieukerken Host: DRD 2684: Cotinus obovatus Raf, and Jurate De Prins for their reviews of 1♂,2♀, em. 4-14 Jul 2008, Gary R. this paper. Graves. (USNM). Distribution (Fig. 1).—Currently Literature Cited known from Baxter, Marion, and Newton counties in north- central Arkansas and Braun, A. F. 1908. Revision of the North American Ozark county in south-central Missouri. species of the genus Lithocolletis Hu¨bner. Etymology.—The specific name, coti- Transactions of the American Entomological Society 34: 269–357, plates 20–24. nivora, is derived from the generic plant of Crocker, R. L. and B. J. Simpson. 1982. Datana the plant host (Cotinus) and the Latin vora perspicua (Lepidoptera: Notodontidae) at- (eat, devour). tacks Cotinus obovatus, a native wood ornamental. Florida Entomologist 65: 375–376. Davis, D.R. 1983. Gracillariidae, pp. 2–11. In ACKNOWLEDGMENTS R.W. Hodges et al. (Eds.). Check List of the Lepidoptera of America North of Mexico. We are indebted to Vichai Malikul, E.W. Classey Ltd. and the Wedge Entomo- Young Sohn, Donald Harvey, and Karolyn logical Research Foundation, London. VOLUME 118, NUMBER 2 253

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