PROC. ENTOMOL. SOC. WASH. 113(1), 2011, pp. 14–30

DISCOVERY OF BOTRANA ([DENIS & SCHIFFERMU¨ LLER]) IN CALIFORNIA: AN INVASIVE SPECIES NEW TO NORTH AMERICA (: )

TODD M. GILLIGAN,MARC E. EPSTEIN,STEVEN C. PASSOA, JERRY A. POWELL,OBEDIAH C. SAGE, AND JOHN W. BROWN

(TMG) Colorado State University, Department of Bioagricultural Sciences and Pest Management, 1177 Campus Delivery, Fort Collins, Colorado 80523, U.S.A. (e-mail: [email protected]); (MEE, OCS) Pest Diagnostics Branch, California Department of Food and Agriculture, Sacramento, California 95832, U.S.A. (e-mail: MEE [email protected], OCS [email protected]); (SCP) USDA/APHIS/PPQ, U.S. Forest Service Northern Research Station and The Ohio State University, Columbus, Ohio 43212, U.S.A. (e-mail: steven.c.passoa@aphis. usda.gov); (JAP) Essig Museum of Entomology, University of California, Berkeley, California 94720, U.S.A. (e-mail: [email protected]); (JWB) Systematic Entomology Laboratory, P.S.I., Agricultural Research Service, USDA, c/o National Museum of Natural History, Washington, D.C. 20013, U.S.A. (e-mail: john.brown@ ars.usda.gov)

Abstract.—The European grape vine , ([Denis and Schiffermu¨ller]), is one of the most destructive pests of grape in the Palearctic Region. Larvae feed on fruit, causing direct damage and promoting secondary infec- tion by Botrytis cinerea Persoon (botrytis bunch rot or gray mold). On September 30, 2009, tortricid larvae damaging grapes in the Napa Valley of California were identi- fied as L. botrana, representing the first records of this species in North America. The presence of L. botrana could have a significant impact on California agriculture— wine, table, and raisin grapes are grown on more than 800,000 acres throughout the state. We provide descriptions and illustrations to aid in the identification of this newly arrived pest, along with a brief history of its discovery. Key Words: Botrytis, grape, European grapevine moth, EGVM, introduction, , Palearctic, , viteana, Vitis DOI: 10.4289.0013-8797.113.1.14

Lobesia botrana ([Denis and Schif- particularly destructive in southern Eu- fermu¨ller]) is an economically important rope and several Mediterranean coun- pest of vineyards throughout the Pale- tries (Roehrich and Boller 1991). The arctic Region (e.g., Bovey 1966, Voigt larvae cause damage to grapes by feed- 1972, Thie´ry and Moreau 2005) but is ing directly on fruit, although the most serious economic losses are due to sec- ondary infection of feeding sites by Bo- * Accepted by Robert R. Kula trytis cinerea Persoon (botrytis bunch rot VOLUME 113, NUMBER 1 15 or gray mold) (e.g., Roehrich and Boller (Nikon Instruments, Melville, NY). The 1991, Fermaud and Le Menn 1992). photograph of the pupal abdominal seg- The threat that this moth poses to Amer- ments and cremaster was taken with a ican agriculture has not gone unnoticed Nikon DXM 1200 camera mounted on an (Pierce 1918), and there have been spo- upright Zeiss Axiomat microscope (Carl radic efforts focused on its exclusion and/ Zeiss Inc., Thornwood, NY). Scanning or detection in North America over the electron micrographs (SEMs) were pre- last few decades. These included a series pared using a JEOL JSM-6500 microscope. of pest alerts, risk assessments, and surveys Some photographs are a combination of in both the United States (Whittle 1985, several layers produced with Helicon Focus Fowler and Lakin 2002, Venette et al. 4.80 software (Helicon Soft Ltd., Kharkov, 2003) and Canada. On September 30, 2009, Ukraine). All photographs were edited us- tortricid larvae found in grape ( ing Adobe Photoshop CS3 Extended L.: Vitaceae) from the Napa Valley of (Adobe Systems Inc., San Jose, CA). California were identified as L. botrana, Morphological terminology and wing representing the first North American re- pattern descriptions follow Gilligan et al. cords of this species. Because more than (2008). Natural history and host infor- 800,000 acres of grapes are cultivated mation is compiled from Ben-Yehuda et al. throughout the state, L. botrana could have a (1993), Bradley et al. (1979), CPC (2007), significant impact on California agriculture. Thie´ry and Moreau (2005), and Venette The purpose of this contribution is to et al. (2003). summarize the literature on the geo- graphic distribution, hosts, life cycle, and RESULTS AND DISCUSSION morphology of L. botrana andtomake Nomenclature this information available to those in- volved in exclusion, detection, and iden- Tortrix botrana Denis and Schiffermu¨ller tification of this species. We also document was described from Vienna, Austria. its discovery in California. Ragonot (1894) proposed the genus Polychrosis with T. botrana as the type MATERIALS AND METHODS species. Over half a century later, Obraztsov Specimens of L. botrana from Europe, (1953) relegated Polychrosis to a subgenus Chile, and California were examined and of Lobesia Guene´e, with L. botrana as its dissected using a Wild M5A stereomicro- only member. Synonyms of L. botrana in- scope (Wild Heerbrugg AG, Switzerland). clude Phalaena vitisana Jacquin and Olin- Dissection methodology follows Brown dia rosmarinana Millie`re (Brown 2005). and Powell (1991) except that some prep- Dufrane (1960) described “flavosquamella” arations were not transferred to xylene and as a form of L. botrana from France. Older instead were mounted in Euparal (Bioquip literature often used the combination Products, Rancho Dominguez, CA). Adults botrana (Gonza´lez 2008). were photographed with a Canon EOS 40D Authorship of the species name botrana digital SLR camera (Canon U.S.A., Lake is unequivocally attributed to Denis & Success, NY) mounted on a Visionary Schiffermu¨ller even though their names Digital BK Lab System (Visionary Digital, do not appear on the original work. Hence, Palmyra, VA). Photographs of genitalia per Recommendation 51D of the Interna- and larval cuticles were taken using a Nikon tional Code of Zoological Nomenclature DXM 1200 digital camera mounted on a (International Commission on Zoolog- Nikon Labophot2 compound microscope ical Nomenclature 1999), the authors’ 16 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON names ...“should be enclosed in square Service for Agrifood Health and Quality brackets to show the original anonymity.” reported L. botrana in Argentina at two Unfortunately, this convention is too fre- locations in the Maipu´ Department, Men- quently ignored. doza Province, close to the Chilean border Lobesia botrana has a wide variety of (SENASA 2010). common names in several languages (see Larval Hosts and Damage list in Gonza´lez 2008). English common names for L. botrana include: European Lobesia botrana is one of the most grapevine moth (EGVM), European grape important pests of grape (Vitis vinifera) moth, grape berry moth, grapevine in the Palearctic (Bovey 1966, Roehrich moth, vine moth, European vine moth, and Boller 1991). Larvae are polypha- grape leaf roller, and grape fruit moth gous and have been recorded from over (Meijerman and Ulenberg 2000, CPC 40 species of in the following 2007); several of these names are shared families: Actinidiaceae, Araliaceae, As- with Eupoecilia ambiguella (Hu¨bner), teraceae, Berberidaceae, Caprifoliaceae, another European tortricid grape pest. Caryophyllaceae, , Ebenaceae, When common names are necessary, Ericaceae, Grossulariaceae, Lamiaceae, we suggest using European grape vine Liliaceae, Menispermaceae, Oleaceae, moth for L. botrana and European grape Punicaceae, Ranunculaceae, Rhamnaceae, berry moth for E. ambiguella, or avoiding Rosaceae, Thymeleaceae, and Vitaceae. A the issue completely by using scientific partial host list is presented in Table 1. nomenclature. Preference for V. vinifera may have evolved only recently as damage to grape Geographic Distribution by L. botrana was not reported until the Lobesia botrana is native to the Pa- early part of the 20th century (Marchal learctic Region and is widely distributed 1912, Thie´ry and Moreau 2005). Female in Western Europe, Central Asia, and L. botrana are attracted to volatiles of both northern Africa (Razowski 2003, CPC Vitis and Daphne (Tasin 2005) but prefer 2007). Records from Japan (Bae and to oviposit on Daphne rather than Vitis Komai 1991) and eastern Africa (Kenya, when given a choice (Maher and Thie´ry Ethiopia, and Eritrea) are likely due to 2006). As a result, several authors (e.g., inadvertent human introductions (CPC Bovey 1966, Tasin 2005, Thie´ry and 2007). North American records of L. Moreau 2005, Maher and Thie´ry 2006) botrana from the mid- to late-1800s are have hypothesized that misidentifications of L. (Thymelaeaceae) is the native host (Clemens) (Kearfott 1904), a native North plant for L. botrana. Polyphagy may per- American grape-feeding tortricid that is sist because hosts other than Vitis provide extremely similar morphologically to L. better nutritional value. Thie´ry and Moreau botrana. (2005) demonstrated that individuals Lobesia botrana was first discovered feeding on alternate hosts had lower larval in the Americas from Chile in April mortality, shorter development times, 2008, where it was reported feeding on higher pupal weight, and increased female grape by the Chilean Department of fecundity and mating success. Agriculture (Gonza´lez 2008). Subse- Larvae of L. botrana damage grape by quently, it spread to all grape growing feeding on flowers, buds, and fruit. First regions of that country (SAG 2010), and generation larvae feed on flower buds, re- in March 2010, the Argentinean National sulting in reduced yields, whereas second VOLUME 113, NUMBER 1 17

Table 1. Documented host plants for L. botrana.

Family Genus/species Common name

Actinidiaceae Planch. kiwi Araliaceae Hedera helix L. English ivy Asteraceae Tanacetum vulgare L. common tansy Berberidaceae Berberis vulgaris L. common barberry Caprifoliaceae Lonicera tatarica L. Tatarian honeysuckle Caprifoliaceae Viburnum lantana L. wayfaringtree Caryophyllaceae Dianthus L. carnation Cornaceae mas L. Cornelian cherry Cornaceae Cornus sanguinea L. bloodtwig dogwood Cornaceae Cornus L. dogwood Ebenaceae Diospyros kaki L. f. Japanese persimmon Ebenaceae Diospyros virginiana L. common persimmon Ericaceae Arbutus unedo L. strawberry tree Grossulariaceae nigrum L. European black currant Grossulariaceae Ribes rubrum L. cultivated currant Grossulariaceae Ribes uva-crispa L. European gooseberry Lamiaceae Rosmarinus officinalis L. rosemary Liliaceae Urginea maritima (L.) Baker red squill Menispermaceae Menispermum canadense L. common moonseed Oleaceae Ligustrum vulgare L. European privet Oleaceae Ligustrum japonicum L. Japanese privet Oleaceae Olea europaea L. Oleaceae Syringa vulgaris L. common lilac Punicaceae Punica granatum L. Ranunculaceae L. evergreen clematis Rhamnaceae Ziziphus jujuba (L.) Karst. common jujube Rosaceae Malus pumila Mill. apple Rosaceae (L.) L. sweet cherry Rosaceae L. European plum Rosaceae Prunus dulcis (Mill.) D.A. Webb sweet almond Rosaceae Prunus persica (L.) Batsch var. nucipersica nectarine (Suckow) C.K. Schneid. Rosaceae Prunus salicina Lindl. Japanese plum Rosaceae L. blackthorn Rosaceae Pyrus communis L. common pear Rosaceae Rubus caesius L. European dewberry Rosaceae Rubus fruticosus L. [excluded] shrubby blackberry Rosaceae Rubus L. raspberry Thymeleaceae Daphne gnidium L. flax-leaved daphne Thymeleaceae Thymelaea hirsuta (L.) Endl. thymelaea Vitaceae Parthenocissus quinquefolia (L.) Planch. Virginia creeper Vitaceae Vitis vinifera L. wine grape

and third generation larvae feed on rip- cinerea (e.g., Roehrich and Boller 1991, ening and mature grapes, respectively Fermaud and Le Menn 1992). Economic (Roehrich and Boller 1991). The most thresholds for L. botrana in grape vary significant economic losses are due not with climatic conditions, type of grape to direct damage to berries but to sec- (wine or table), and cultivar (Roehrich ondary infection of feeding sites by B. and Boller 1991). The species also is 18 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Figs. 1–4. Adult wing patterns. 1–2, Lobesia botrana; 3–4, Paralobesia viteana

considered a minor pest of some orna- as five in Central Asia (Filip 1986, CPC mental and greenhouse plants and has 2007). There are at least three and possibly been reported infesting pear (Pyrus com- four generations in Chile (Gonza´lez 2008). munis L.; Rosaceae) orchards in Israel The lower temperature threshold for egg, (Ben-Yehuda et al. 1993). larval, and pupal development is approxi- mately 8 °C (Gabel and Mocko 1984). Life Cycle and Biology The following summary of the life Lobesia botrana completes 2–3 gen- cycle on grape is derived from Bovey erations annually in southern Europe, al- (1966), Bradley et al. (1979), CPC though the number of generations varies (2007), Masante-Roca et al. (2007), and from one in northern Europe to as many Meijerman and Ulenberg (2000). Females VOLUME 113, NUMBER 1 19

Figs. 5–9. Male and female genitalia. 5, L. botrana female; 6, L. botrana male; 7, L. botrana male, arrow denotes gap in spines on valva; 8, P. viteana male; 9, P. viteana female.

of the first generation deposit eggs singly the first and second generations pupate in or in groups of two or three on buds, rolled leaves or inflorescences tied with pedicels, and flowers; those of the sec- silk. Pupae complete development in ond and third generations deposit single approximately 12–14 days, or 130 degree- eggs on individual grape berries. Eggs days, for non-diapausing individuals. Dia- hatch in approximately 5–10 days or pausing individuals of the third or subsequent 75 degree-days above a 10 °C threshold. generations pupate under bark, in the soil, Larvae complete five instars, with the first or under leaf litter; adults emerge the fol- generation feeding on flowers and buds, lowing spring. the second generation feeding within a Morphology single unripened grape berry, and the third and subsequent generations feeding on Egg (Figs. 20–22).—The egg of ripened berries. Larval development is com- L. botrana, originally illustrated by pleted in approximately 20–28 days or 170 Silvestri (1912), is elliptical, flattened, degree-days for larvae feeding on flowers and slightly convex. Each egg is approx- and 225 degree-days for larvae feeding imately 0.65–0.90 mm long by 0.45–0.75 on berries. Non-diapausing individuals of mm wide (CPC 2007). The chorion is 20 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Figs. 10–16. Lobesia botrana larvae. 10, Larva feeding on Botrytis cinerea; 11, Larva on grape; 12, Typical damage to grapes (courtesy Roberto H. Gonza´lez, Universidad de Chile); 13, Details of head and prothoracic shield; 14, Dorsal aspect of segment A9 showing D2s on “saddle” pinaculum, and D1 and SD1 on same pinaculum; 15, Ventral aspect of segment A8 showing relative spacing of V1 setae; 16, Ventral aspect of segment A9 showing relative spacing of V1 setae. either smooth or there is a slight poly- substrates may affect the coloration (H. gonal reticulation on the border and Nadel pers. comm.). around the micropile (CPC 2007). When No morphological characters are newly laid, eggs are translucent pale yellow, available to separate eggs of L. botrana eventually turning “opalescent” gray (Mei- from related species in the Olethreuti- jerman and Ulenberg 2000), with the em- nae. However, many species of Tortricinae bryo becoming visible during incubation. (i.e., Archipini and Sparganothini) oviposit Because the egg is semi-transparent, dark in large overlapping clusters (Powell and VOLUME 113, NUMBER 1 21

Figs. 17–22. Lobesia botrana eggs and pupae. 17, Pupa and cocoon; 18, Pupa; 19, Pupa, dorsal aspect of A10 with patch of spines; 20, Egg on grape; 21, Egg on grape; 22, Embryo inside of translucent egg.

Common 1985, Horak 1991). This ovi- approximately 1.0 mm in length. The position pattern characterizes several head is black to dark brown, and the common Californian tortricid pests such paler prothoracic shield is concolorous as Platynota stultana Walsingham, Arg- with the rest of the body. The mature yrotaenia franciscana (Walsingham), and larva (Figs. 10–12) is 10–15 mm long Epiphyas postvittana (Walker). Eggs of L. and varies in color from light yellowish botrana arelaidsinglyorinsmallclumps, green to pale brown. The head is brown to neverinamass. light yellowish brown to honey colored, Larva (Figs. 10–16, 23–29).—The the antennae and thoracic legs are brown first instar larva is yellowish green and to black, and the prothoracic shield is 22 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON variably shaded with dark brown to black on head passes through AF2 (Fig. 24); on the posterior and lateral margins. All L pinaculum on T1 horizontal, not ex- instars have a dark stemmatal area and tending beneath spiracle (Fig. 23); SV genal dash. Prepupae are colored a “dull groups on A1, 2, 7, 8, 9 with 3:3:3:2:2 dark purple” (H. Nadel pers. comm.). setae (Fig. 23); SD2 on A1–8 absent Irigaray et al. (2006) measured head (Fig. 23); distance between V setae on capsule widths for each instar. A9 approximately 1.5–2.03 the distance Important structural features of the L. between V setae on A8 (Fig. 29); dis- botrana larva include: mandibles with- tance between D1 setae on anal shield out inner teeth (sensu Passoa 1985) or equal to the distance between D1 and a retinaculum (Fig. 25); distance be- SD1 (Fig. 23); anal comb with 5–6 teeth tween P1 and AF2 on head equal to in California individuals (Fig. 29), other distance between P1 and P2 (Fig. 24); authors (e.g., Swatschek 1958) report a horizontal line connecting the P2 setae 6–8 teeth; and body spicules relatively

Figs. 23–25. Lobesia botrana larval details. 23, Complete setal map; 24, Head with setal map; 25, Mandible. VOLUME 113, NUMBER 1 23 dense (at 2003 or more) (Figs. 28–29). Lobesia botrana belongs to the sub- See Figs. 23–24 for a complete setal map. family , whose larvae can In addition to the above, Swatschek usually be recognized by a combination (1958) stated the abdominal prolegs of three characters: L group on the pro- have 35 biordinal crochets in a complete thorax trisetose, D2 setae of A9 closely circle and the anal proleg has 25 cro- spaced or joined on “saddle” pinaculum, chets, also biordinal. Four setae are and A9 with the D1 and SD1 setae fused present on the ventral portion of the anal on a single pinaculum (Figs. 14, 28). proleg (called the “caudal disc” in the Other common tortricid pests in Cal- translation by Ericson 1960). ifornia (P. stultana, A. franciscana, and

Figs. 26–29. SEMs of L. botrana larva. 26, Head; 27, Spinneret; 28, Dorsal aspect of segments A9– 10 with anal shield; 29, Ventral aspect of segments A9-10 showing spacing of V1 setae, 4 setae on the anal proleg, and anal comb with 5 teeth. 24 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

E. postvittana) belong to the subfamily patterns might be more useful. We rec- Tortricinae, whose larvae have D1 and ommend rearing the immature stages to an SD2 of A9 on separate pinacula (see adult or using molecular methods if ac- Gilligan and Epstein 2009). curate larval identifications are needed for The key in MacKay (1959), or the quarantine decisions in areas outside of simplified version in Passoa (2008), can California and/or on hosts other than be used to separate L. botrana larvae grape. Color photographs of the immature from many other Olethreutinae in the stages without vouchers specimens cannot United States. Because the A and L setae be identified. of the head are not in a straight line, all Pupa (Figs. 17–19).—The most ac- thoracic legs are concolorous, and the curate pupal description of L. botrana SV group on A7 is trisetose, L. botrana was given by Patocka and Turca´ni. will group with Nearctic species of En- (2005). Like many tortricids, the pupa is dothenia, Lobesia, and Paralobesia us- initially greenish brown and later turns ing either of these keys. The larva of L. dark brown; however, cast pupal skins botrana also lacks a dark contrasting are somewhat unusual in retaining a patch on the prothoracic shield (although greenish tint on the anterior abdominal a thin marginal line may be present) and segments. The average length of male extra setae on the abdominal segments. and female pupae is 5.5 mm and 7.0 mm, Paralobesia viteana (Clemens) is a na- respectively(CPC2007).Importantstruc- tive North American pest of grapes with tural features of L. botrana include: head an almost identical larval morphology unmodified, without projections (Fig. 18); to L. botrana. The two species presently clypeus with two pairs of setae; A4 and A5 have separate distributions: P. viteana with 22–24 spines between the D2 setae; occurs in the eastern U.S., ranging as dorsum of A10 with a patch of spines (Fig. far west as Colorado, while L. botrana is 19) and no setae present on the anal rise currently restricted to California. Although (Fig. 19) (Patocka and Turca´ni 2005). The it appears that the brown to greenish cremaster is fan-shaped with a weakly yellow antenna of P. viteana (Ensminger emarginate caudal margin (Fig. 19) 1958) differs from the black or dark (Meijerman and Ulenberg 2000). brown antenna of L. botrana,thisdiffer- On agriculturally important plants in ence needs to be tested with a large series North America, most pupae with two of specimens. Ensminger (1958) and rows of abdominal spines are those of MacKay (1959) illustrate the larvae of Tortricidae. Mosher’s (1916) key to fami- P. viteana. lies is still the standard, although recent Should L. botrana spread to areas workers have modified this diagnosis outside of California, or become com- slightly (Horak 1991, Passoa 2008), and her mon on hosts other than grape, larval classification is outdated. Mosher (1916) identification will be difficult. Charac- examined the pupa of L. botrana and rec- ters in the published (MacKay 1959) and ognized it as distinct from P. viteana.The unpublished literature (USDA/APHIS/ broad cremaster lacking thick curved hooks PPQ training aids) such as attenuated at the lateral margin, the presence of spines adfrontal areas, or the spiracle size com- on A9, the lack of setae on the anal rise and pared to the SD1 pinaculum, seem too presence of a spine patch on A10 was used variable or difficult to interpret to be to define Lobesia (= Polychrosis). useful for identification of these closely As with the larvae, L. botrana pupae related taxa. Minute differences in crochet are morphologically similar to those of VOLUME 113, NUMBER 1 25

P. viteana. Both species have a patch (or strong spines on ventral margin; cucullus weakly defined row) of spines on the densely setose, separated from sacculus dorsum of A10 (Fig. 19), but they can be by distinct gap in row of ventral spines separated by the number of spines on the (Fig. 7); sacculus weakly concave post- anterior row of segments A4 and A5: medially; phallus small; cornuti absent. 22–24 spines between the D2 setae in Female genitalia (Fig. 5) are character- L. botrana (Patocka and Turca´ni 2005), ized by a long, slender ductus bursae that never more than 15 in P. viteana. is undifferentiated from the corpus bur- Larvae of L. botrana spin an opaque, sae, gradually expanded anteriorly, and white cocoon approximately 8–10 mm an unusual, elongate, somewhat feather- in length that is usually at least partially shaped signum. covered in frass. The presence of a co- Lobesia botrana is similar in size and coon can be used to separate L. botrana wing pattern to several species of Pa- pupae from other common California ralobesia, specifically Paralobesia vi- tortricid grape pests that do not spin teana (Figs. 3–4), which is a native pest a cocoon, such as P. stultana and A. of grapes in eastern North America. The franciscana. two species can be separated by genitalic Adult (Figs. 1–2, 5–7).—Forewing structures: P. viteana has a sclerotized length ranges from 4.5–8.5 mm (Bradley lobe projecting from the ventral base of et al. 1979). Forewing pattern (Figs. 1–2) the male cucullus that is absent in all exhibits little variation and no sexual other Nearctic olethreutines (Fig. 8), and dimorphism. Forewing pattern is as fol- the female corpus bursae lacks a signum lows: ground color cream; interfascial and has two small lobelike anterior ac- areas overlaid with leaden gray; costal cessory bursae (Fig. 9) (Gilligan et al. strigulae cream, well defined; fasciae 2008). Only three species of Paralobesia brown to dark brown; subbasal fascia have been recorded from the West Coast. well defined, with black scaling medi- Paralobesia palliolana (McDunnough) ally; median fascia well defined, with was collected in the late 1990’s near triangular medial projection often suf- Olympia, Washington (E. LaGasa pers. fused with black scaling; postmedian comm.). An apparently undescribed spe- fascia broken, forming pretornal patch cies of Paralobesia was reared from along dorsum with cluster of black Calocedrus sp. (Cupressaceae) in California scales; postmedian band forming large (J. Powell unpubl.). Another undescribed brown patch along termen; apex often species of Paralobesia was discovered in with conspicuous black dot; termen Oregon as a non-target species in an E. outlined in cream; fringe brown. The postvittana pheromone trap on August males lack a forewing costal fold. The 6, 2009 (R. Worth pers. comm.); it is male hind wing is whitish with a brown unknown if this species is native to or periphery, while the female hind wing is established in Oregon or present in completely brown. California. All of the species of Paralobesia Male genitalia (Figs. 6–7) can be mentioned here can be separated from L. distinguished by a combination of the botrana by features of the male and female following characters: socii short, lateral, genitalia; it is unknown if any of them are apex with numerous setae; uncus re- attracted to L. botrana pheromone. Other duced to small bilobed hump on tegu- species of Paralobesia in the eastern U.S. men; gnathos weakly sclerotized; valvae are treated in detail by Gilligan et al. long and narrow with dense row of (2008). 26 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

In California, common tortricid pests Diagnostics Branch for identification. recorded feeding on grape include P. DNA was extracted from several larvae, stultana, A. franciscana,andE. post- amplified and sequenced. On 30 Sep- vittana. Gilligan and Epstein (2009) tember, barcode sequences (650 base- provided diagnostic characters for these pair region of the mitochondrial gene three species, the adults of which are cytochrome oxidase I) from the unknown easily distinguished from L. botrana by larvae were compared with sequence data wing pattern and genitalic structure of a known L. botrana specimen obtained (e.g., see Brown et al. 2010, Gilligan et al. from Spain in 2009 by T. Gilligan and 2010). sequenced by USDA-CPHST Mission Two other species of Lobesia, Lobesia Laboratory. The two sequences were carduana (Busck) and Lobesia bi- identical. One adult and several larvae cinctana spiraeae (McDunnough), are were received by J. Brown at the USDA present in North America. The former Systematic Entomology Laboratory on is a leaf-roller on thistle (Asteraceae) in 8 October where the adult was con- the eastern United States. The latter was firmed as L. botrana andthesixlarvae described as Polychrosis spiraeae by identified as Lobesia sp. CDFA imme- McDunnough (1938) from individuals diately initiated pheromone trapping in feeding in flower heads of Spiraea grape-growing regions of Napa and (Rosaceae) in Nova Scotia and was rele- Sonoma counties. The discovery of gated to a subspecies of Lobesia bicinctana L. botrana in California was informally (Duponchel) by Obraztsov (1953). Both reported in several newspaper articles Lobesia species can be distinguished from and press releases on 12 and 13 October. L. botrana by genitalia characters. The Adult L. botrana were collected in phero- Palearctic L. bicinctana is illustrated by mone traps in Napa County through late Razowski (2003), and L. carduana is October 2009. illustrated by Gilligan et al. (2008). Larvae of L. botrana were un- knowingly collected in California the Discovery of Lobesia botrana previous year. On September 11, 2008, in California several larvae were found in grape The introduction of L. botrana into clusters in Napa Valley. A second series the United States was predicted as early of larvae were collected on 17 Septem- as 1904 by W. D. Kearfott who wrote: “It ber. The larvae, originally thought to be is not at all unlikely that the European those of orange tortrix, Argyrotaenia botrana will be at some time introduced franciscana (Walsingham), were sent to in this country with imported grape M. Epstein for identification. The larvae vines...” Kearfott’s prediction came were confirmed as Tortricidae but could true on September 15, 2009 when sev- not be identified to genus or species. eral Lepidoptera larvae were collected Attempts to rear the larvae to adults were from a vineyard 18 km northwest of Napa, unsuccessful as they died as pupae in Napa County, California. Napa County cocoons during the winter, sealed in officials at the site noted that every a growth chamber. Immediate molecular grape cluster in the vineyard was dam- diagnosis of the larvae was not possible aged and that many clusters were infected because public barcode reference se- with Botrytis. Larvae were forwarded to quences of L. botrana were not available M. Epstein at the California Depart- in 2008, and attempts to obtain reference ment of Agriculture’s (CDFA) Plant Pest larvae for P. viteana from the eastern VOLUME 113, NUMBER 1 27

United States and L. botrana from Eupoecilia ambiguella sometimes co- Europe were unsuccessful. In October exists with L. botrana in Europe although 2009, DNA sequence data from larvae the distribution and abundance of each captured in 2008 were found to match species is greatly influenced by climate (e.g., 100%) sequence data of larvae (Roehrich and Boller 1991). Morpho- captured from the original collecting site logical differences between the two were in 2009. provided by Silvestri (1912). Regulatory A statewide survey of California for L. officials should be diligent in their ef- botrana was initiated in early 2010. As forts to exclude E. ambiguella which of October 2010, individuals of L. botrana could follow L. botrana into North have been collected from the following American vineyards, especially in cooler California counties (dates represent the first areas. collection date): Fresno, April 27, 2010; Control and management of invasive Mendocino, April 26, 2010; Merced, May species begin with their early detection 10, 2010; Monterey, May 10, 2010; Napa, and accurate identification. The need to September 17, 2008; San Joaquin, August support local moth surveys in analyzing 2, 2010; Santa Clara, September 15, 2010; exotic pest establishments has already Santa Cruz, September 1, 2010; Solano, been demonstrated (Brown et al. 2010). April 19, 2010; and Sonoma, March 29, Hence, entomologists at the local, state, 2010. A total of 100,945 individual L. and federal levels are encouraged to botrana have been captured in California cooperate in the continued monitoring through October 2, 2010 (K. Hoffman pers. and management of this and other po- comm.). Interception records from neither tentially invasive pests. APHIS nor CDFA provide evidence of the origin, pathway, or date of arrival of P. ACKNOWLEDGMENTS botrana into California. Portions of this project were funded CONCLUSIONS through a cooperative agreement with Increased globalization has led to California Department of Agriculture, a concomitant increase in the potential Colorado State University, and USDA- transport, introduction, and establish- CPHST under the supervision of Terrence ment of plant and species around Walters. We thank Roberto Gonza´lez, the world. Invasive species cost the U.S. Universidad de Chile, for specimens, in- billions of dollars per year in agricultural formation on L. botrana in Chile, and the and forest ecosystem losses (Pimentel use of Fig. 12. Luis Miguel Torres-Vila, et al. 2000). The introduction of pests Servicio de Sanidad Vegetal, Spain, and such as L. botrana into North America Frans Groenen, Luyksgestel, Netherlands, represents not only potential economic graciously provided specimens of L. impacts to agroecosystems but also may botrana from Europe for sequencing. result in costly quarantine actions with Hannah Nadel and Nada Carruthers, trading partners. The European grape USDA-APHIS-PPQ, provided specimens vine moth may negatively affect grape of L. botrana from their laboratory production in California and elsewhere if cultures for morphological analysis. Nor- it proves able to spread from the Napa man Barr, USDA-CPHST Mission Labo- Valley to other grape growing regions. ratory, provided sequence data. Richard The association with stone and pome Worth, Oregon Department of Agri- fruits, although rare, is equally disturbing. culture, and Eric LaGasa, Washington 28 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

State Department of Agriculture, pro- Brown, J. W., M. E. Epstein, T. M. Gilligan, S. C. vided details on West Coast Paralobesia. Passoa, and J. A. Powell. 2010. Biology, Joel Aronoff and Susan Ellis, USDA- discovery, and history of the light brown apple moth, Epiphyas postvittana (Walker) (Lepi- APHIS-PPQ, provided imaging equipment doptera: Tortricidae: Archipini) in California: used to photograph larval characters. an example of the importance of local faunal Specimens of P. viteana were loaned by surveys to document the establishment of exotic the Charles A. Triplehorn Col- . American Entomologist 56(1): 34–43. lection at The Ohio State University. Jon CPC (Crop Protection Compendium). 2007. CAB Lewis, USDA-SEL, tracked down and International, Wallingford, UK. http://www. cabicompendium.org/cpc/home.asp [accessed copied needed references. The following, 29 October 2009]. and two anonymous reviewers, pro- Dufrane, A. 1960. Microle´pidopte`resdelafaune vided helpful reviews of the manu- belge. Bulletin de l’Institut Royal des Sciences script: Thomas Henry, USDA-SEL; Boris Naturelles de Belgique 36(29): 1–16. Kondratieff, Colorado State University; Ericson, R. 1960. Unpublished English translation Robert Kula, USDA-SEL; Paul Opler, of Swatschek B. 1958. Die larvalsystematik der Wickler (Tortricidae und Carposinidae). Colorado State University; and Kevin Abhandlungen Zur Larvalsystematik der In- Hoffman, California Department of Food sekten nr. 3. Akademie-Verlag, Berlin, Germany. and Agriculture. The comments and rec- 206 pp. ommendations of the reviewers signifi- Ensminger, L. G. 1958. Identification of stored cantly improved the manuscript, and the product insects by the micromorphology of authors are grateful for this assistance. the exoskeleton. VIII. Moth larvae. Journal of the Association of Official Agricultural Chemists 41: 704–738. Literature Cited Fermaud, M. and R. Le Menn. 1992. Trans- mission of Botrytis cinerea to grapes by Bae, Y.-S and F. Komai. 1991. A revision of the grape berry moth larvae. Phytopathology 82: Japanese species of the genus Lobesia Guene´e (Lepidoptera, Tortricidae), with 1393–1398. doi:10.1094/Phyto-82-1393 description of a new subgenus. Tyo to Ga Filip, I. 1986. Breeding zones of the grape moth 42: 115–141. (Lobesia botrana Den. & Schiff.) in Romania. Ben-Yehuda, S., Y. Izhar, M. Wysoki, and Q. Probleme de Protectia Plantelor 14: 25–30. Argaman. 1993. The grape berry moth, Lobesia Fowler, G. and K. Lakin. 2002. Risk assessment: botrana (Denis & Schiffermu¨ller) (Lepidoptera: Vine moth, Lobesia botrana (Denis and Tortricidae), in pear orchards in Israel. Inter- Schiffermu¨ller), (Lepidoptera: Tortricidae). national Journal of Pest Management 39: 149– USDA-APHIS-CPHST Internal Report Ra- 151. doi: 10.1080/09670879309371780 leigh, North Carolina. 15 pp. Bovey, P. 1966. Super-famille des Tortricoidea, Gabel, B. and V. Mocko. 1984. Forecasting the pp. 456–893. In A. S. Balachowsky, ed. En- cyclical timing of the grape vine moth, tomologie applique´e a l’agriculture. Volume Lobesia botrana (Lepidoptera, Tortricidae). 2(1), Lepidopte`res. Mason & Cie, Paris. Acta Entomologica Bohemoslovaca 81: 1–14. 1057 pp. Gilligan, T. M., D. J. Wright, and L. D. Gibson. Bradley, J. D., W. G. Tremewan, and A. Smith. 2008. Olethreutine of the Midwestern 1979. British Tortricoid Moths, Tortricidae: United States, an Identification Guide. Ohio Olethreutinae. The Ray Society, London. Biological Survey, Columbus, Ohio. 334 pp. 336 pp. Gilligan, T. M. and M. E. Epstein. 2009. LBAM Brown, J. W. 2005. World Catalogue of Insects. ID: Tools for Diagnosing Light Brown Apple Volume 5, Tortricidae (Lepidoptera). Apollo Moth and Related Western U.S. Leafrollers Books, Stenstrup, Denmark. 741 pp. (Tortricidae: Archipini) [CD-ROM]. USDA- Brown, J. W. and J. A. Powell. 1991. Systematics APHIS. of the Chrysoxena group of genera (Lepi- Gilligan, T. M., S. C. Passoa, and M. E. Epstein. doptera: Tortricidae: Euliini). University of 2010. European grapevine moth Lobesia bo- California Publications in Entomology 111: trana (Denis & Schiff.) screening and iden- 1–129. tification aid, pp. 6–11. In 2010 Taxonomic VOLUME 113, NUMBER 1 29

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