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Faculty Publications: Department of Entomology Entomology, Department of

2019

A NEW PEST OF (DIPTERA: ) ON SOYBEAN (FABACEAE) IN , WITH A DESCRIPTION OF THE

Raymond Gagne

Junichi Yukawa

Ayman K. Elsayed

Anthony J. McMechan

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This Article is brought to you for free and open access by the Entomology, Department of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications: Department of Entomology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. PROC. ENTOMOL. SOC. WASH. 121(2), 2019, pp. 168–177

A NEW PEST SPECIES OF RESSELIELLA (DIPTERA: CECIDOMYIIDAE) ON SOYBEAN (FABACEAE) IN NORTH AMERICA, WITH A DESCRIPTION OF THE GENUS

urn:lsid:zoobank.org:pub:E94E2A94-0253-4593-A757-DA57A08C6178

RAYMOND J. GAGNE´,JUNICHI YUKAWA,AYMAN K. ELSAYED, AND ANTHONY J. MCMECHAN

(RJG) Systematic Entomology Laboratory, Agricultural Research Service, U.S. Department of Agriculture, c/o Smithsonian Institution MRC-168, P.O. Box 37012, Washington, DC 20013-7012, USA (corresponding author, [email protected]. gov); (JY) Entomological Laboratory, Faculty of Agriculture, Kyushu University, Fukuoka 819-0395, Japan ([email protected]); (AKE) Department of Applied Entomology, Faculty of Agriculture, Alexandria University, Alexandria, Egypt, presently in Laboratory of Systems Ecology, Faculty of Agriculture, Saga University, Saga 840-8502, Japan ([email protected]; (AJM) University of Nebraska ─ Lincoln, Eastern Nebraska Research and Extension Center, 1071 County Road G, Ithaca, NE 68033, USA ([email protected]

(RJG) urn:lsid:zoobank.org:author:581F6F92-83AA-476E-A5CE-A1B814D925E8 (JK) urn:lsid:zoobank.org:author:989FF55B-6273-4B73-B739-865406449BAE (AKE) urn:lsid:zoobank.org:author:21B0814A-3955-463D-817F-9E2F73764E9E (AJM) urn:lsid:zoobank.org:author:996A9F8D-D941-4255-945C-F86804FF4A33

Abstract.—A new species, Resseliella maxima Gagne´, is reported that feeds on the lower stems of soybean, Glycine max (L.) Merr. (Fabaceae) in Nebraska, Iowa, South Dakota and Minnesota. It is described and illustrated and compared in detail with other Resseliella spp. DNA data support its status as a new species. A general description is given for Resseliella. Key Words: , , Glycine max DOI: 10.4289/0013-8797.121.2.168

A new species of gall (Diptera: revealed orange larvae feeding within Cecidomyiidae) was recently discovered and at the leading edge of these darkened feeding on the stems nearest the base areas (Fig. 1). Initial feeding appeared to of soybean, Glycine max (L.) Merr. be confined to the phloem with larvae (Fabaceae) in Nebraska, Iowa, South moving into the xylem and pith over Dakota and Minnesota. Externally, in- time. Since 2011 this cecidomyiid has fested areas of the stems were dark brown been associated with hail-damaged or or black. Dissection of infested disease-compromised soybean plants. VOLUME 121, NUMBER 2 169

Signs of larval infestation occurred at the (2017). Most species have been reared end of the growing season in late August but some are known only from speci- so raised little concern about economic mens caught in flight. The genus is an- losses. In 2018 visible signs of dead or atomically rather uniform in gross aspect dying plants infested with the soybean and has not yet undergone a critical re- gall midge were observed in late June. A view. Nonetheless, specific-level attri- portion of the fields surveyed in 2018 had butes of both sexes, pupae and larvae significant levels of damage with the are available and elucidated here. Many greatest frequency of dead plants at the species live under bark or in flower field edge, dissipating with distance to- heads, but some form simple , e.g., wards the center of the field. In addition, swellings of midribs or simple blister heavily impacted areas were often next galls of tuliptree (Magnoliaceae) (Gagne´ to waterways and ditches with dense veg- 1989). Important pest species include etation, suggesting that such areas may three species from Japan, Resseliella serve as refugia for overwintering larvae. soya (Monzen) that lives inside leaf veins Symptomatic soybean plants were sub- and petioles of soybean, Resseliella yagoi mitted to diagnostic clinics in Ne- Yukawa and Sato that feeds in braska, Iowa and South Dakota for plant (Rosaceae), and Resseliella resinicola diseases. A number of plant pathogens Sanui & Yukawa in resin of cryptome- were found; however, a portion of plants ria (Taxodiaceae), and also the Euro- that were submitted had no detectable plant pean Resseliella oculiperda (Ru¨bsaamen) diseases, raising concerns about the status that attacks fresh grafts of fruit trees, of this as a primary pest of soybean. the South African Resseliella proteae The new species belongs to Res- Gagne´ that lives in flowerheads of pro- seliella, a cosmopolitan genus of 56 teas (Proteaceae) and the Australian known species. A list with their hosts Resseliella xanthorrhoeae Kolesik that can be found in Gagne´ and Jaschhof feeds at the base of stems of dianellas

Figs. 1–2. Resseliella maxima. 1, Larvae in soybean stem. 2, Adult female. 170 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

(Xanthorrhoaceae). The last-named spe- niques outlined in Gagne´ (1989). A cies lives in association with a fungus as glossary of adult morphological terms does the new species (Kolesik & Baker can be found in Gagne´ (2018) and 2013). anatomy of the third instar follows Gall midge larvae have piercing-sucking Gagne´ (1989). Drawings were made by mouthparts and feed on a liquid diet. Upon RJG with the use of a camera lucida at- reaching maturity all Resseliella lar- tached to a Wild phase contrast micro- vae, including species that live inside scope. The holotype and paratypes are plants, drop to the soil where they pupate. deposited in the insect collection of the Adults emerge the same or the next year National Museum of Natural History in depending on the number of generations Washington, DC (USNM). per year. Adults are easily keyed to genus Total DNA was extracted from the in the key to genera in Gagne´ (2018), a whole body of three third instars each of main character being their robust and Resseliella soya and the new species distinctively shaped claws with slightly found feeding on lower stems of G. max decumbent tips (Figs. 6-7). Perhaps half in Nebraska. A 472bp fragment of the the species have strongly marked anten- mitochondrial gene cytochrome oxidase nae, wings and legs. The pattern on the subunit I (COI) was sequenced and antennae and legs are stereotypical but the aligned following Elsayed et al. (2017), more complicated and easily obscured using the following primer set: Forward: pattern on the wings appears to differ J-1718 (5’– GGA GGA TTT GGA AAT among species. Larvae are distinctive for TGA TTA GTT CC–3’) (Simon et al. the two large lobes on the terminal seg- 1994) and reverse: COIA (5–CCC GGT ment that each bear a short-corniform AAA ATT AAA ATA TAA ACT TC–3) papilla apically and one setose papilla (Funk et al. 1995). The sequences obtained medially at about midlength (Figs. 23-24). were compared using MEGA (version 6.0) The provenance of the new species, (Tamura et al. 2013) and deposited in the whether native or alien, is unknown. Be- DNA Data Bank of Japan (DDBJ), Eu- cause it has only recently been discovered, ropean Molecular Biology Laboratory it might have switched host from another (EMBL), and GenBank nucleotide se- plant, possibly a less important native le- quence databases as accession numbers gume. Resseliella soya is associated with LC437337–LC437339 and LC437340– soybean in Japan but lives inside leaf tis- LC437342 for R. soya and R. maxima, sue or stems and has no fungal associates. respectively. We show here that it is a distinct species morphologically and genetically. RESULTS AND DISCUSSION

MATERIALS AND METHODS Genus Resseliella Seitner On August 1, 2018, emergence cages Gagne´ and Jaschhof (2017) can be were placed over cecidomyiid-infested consulted for a synonymy of Resseliella. soybean plants at Eastern Nebraska Re- The following diagnosis lists the attributes search and Extension Center. Within shared by known species and can serve as 24 hours adults were observed flying a checklist for future species descriptions. in cages and individuals continued to It is based on a survey done for this paper emerge through August 19. Third instars of characters shared by known species in and adults obtained there were mounted published descriptions as well as the for study in Canada balsam using tech- species represented in the USNM. VOLUME 121, NUMBER 2 171

Figs. 3–11. Resseliella maxima. 3, Male , scape through third flagellomere showing banding. 4, Male third flagellomere. 5, Female third flagellomere. 6, Foreclaw. 7, Midclaw. 8, Foreleg showing banding. 9, Hindleg showing banding. 10, Female abdomen, seventh segment to end (ventrolateral). 11, Detail of ovipositor terminus (lateral). 172 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Adult (Fig. 2). Body in life uniformly few short, posterolateral setae on tergite light to dark brown or additionally with 7. Sternites 2-7 with mostly single row antennae and legs light- and dark-banded of posterior setae, 2-3 rows of setae and wings variously light- and dark mixed with a few scales near midlength, patterned. Head: Eyes connate with long these becoming more extensive posteri- eye bridge at vertex; facets circular, orly on sternites 4-7 to reach posterior closely approximated throughout. Occiput row of setae, and pair of closely set with dorsal protuberance bearing 2-3 long anterior trichoid sensilla; sternite 7 addi- setae apically. Antenna: scape with sparse tionally with double row of posterior se- setae ventrally; occiput ringed with sparse tae; sternite 8 narrower than sternite 7, setae; 12 flagellomeres, 12th usually with a with setae and scales on posterior half narrow apical prolongation; male flag- and the pair of trichoid sensilla widely ellomeres (Fig. 4) binodal, first node of spaced. Terminalia (Figs. 13-16): cerci each with one circumfilum, second with convex apically, about as long as hypo- two, circumfila all with uniform moder- proct but often skewed in preparations, ately long loops; female flagellomeres with sparse setae along margin; hypo- (Fig. 5) cylindrical, necks bare, about 1/4 proct subrectangular, slightly to deeply length of nodes. Frons with 4-6 strong se- concave apically, usually concave later- tae on each side. Labella narrow in frontal ally, microtrichose on both surfaces, with view, broad in lateral view, with several 3-4 pairs of short apicoventral setae; ae- strong setae. Palpus 4-segmented with deagus about as long as hypoproct, gently scattered setae, without scales. tapered to rounded apex, with pair of Thorax: Scutum with 4 discrete lon- asetose papillae on each side; gonocoxite gitudinal rows of setae. Scutellum with ovate to bulbous in dorsal view, with group of setae on each side. Pleura with obtuse mediobasal lobe in some species; sparse scales on anepisternum, setae on gonostylus more or less tapered, setulose anepimeron, remaining pleura bare. Wing basally, glabrous and ridged beyond, with (Fig. 2): C broken at juncture with R5;R5 scattered, short setae. curved apically to join C posterior to wing Female abdomen (Figs. 10-11) Ter- apex; Rs incomplete, closer to arculus gites 1-7 generally as for male 1-6 but than to apex of R1; wing fold evident; M4 larger; tergite 7 narrower than 6th; ter- and CuA forming a fork. Legs (Figs. 2, gite 8 much narrower than 7th with short 8-9): slender, elongate; acromere: claws terminal setae and anterior pair of tri- (Figs. 6-7) robust, strongly bent near basal choid sensilla the only vestiture. Ster- third, and with slight downward bend near nites 2-7 generally as for male; sternite 8 apex, always toothed on foreleg, rarely undefined but a pair of widely spaced with additional, finer tooth, mid- and trichoid sensilla evident. Ovipositor hindclaws all toothed or all simple. protrusible, elongate, cylindrical, sur- Male abdomen (Fig. 12): Tergites 1-6 face of both eversible and protrusible entire, rectangular, with single, closely- parts minutely spiculose and sparsely set row of setae along posterior margin, and uniformly covered with short setae, several lateral setae, a pair of widely except bare dorsally immediately pre- spaced anterior trichoid sensilla, and ceding cerci; protrusible part without elsewhere mostly covered with scales; lateral sclerites and 3-7 times the length tergites 7-8 only about a third as long as of the 7th tergite; cerci elongate-ovoid tergite 6, a pair of trichoid sensilla an- with scattered long and short setae, one teriorly the only vestiture except for a pair near terminus thickened, with sockets VOLUME 121, NUMBER 2 173

Figs. 12–14. Resseliella maxima. 12, Male abdomen, sixth through eighth segments (lateral). 13, Cerci (dorsal). 14, Terminalia, cerci not shown (dorsal). Fig. 15, Resseliella soya, same. Fig. 16, Re- sseliella clavula, same. larger than those of remaining setae; thoracic spiracles elongate, pointed. Ab- hypoproct much shorter than cerci with dominal spiracles sessile. Terga 2-8 each two apical setae. with about 5- to 6-branched anterior spines Pupa. Vertex convex, each side with (cf. Kolesik & Baker 2013: fig. 6b) or with long seta on raised base (Fig. 17). Anten- 6 simple spines (cf. Yukawa & Sato 2009: nal bases with short, obtuse anteromedial fig.4e),dorsumelsewhereandpleuraand angles and short apicoventral umbo (Fig. sterna uniformly covered with short spic- 17) anteroventrally. Face smooth. Pro- ules. 174 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON

Fig. 17. Resseliella liriodendri, pupal antennal bases and vertexal papilla. Fig. 18, Resseliella soya, larval spatula. Fig. 19, Resseliella clavula, larval spatula. Figs. 20-24. Resseliella maxima. 20, Larval spatula. 21, Larval fifth abdominal segment (left half, ventral). 22, Same (right half, dorsal). 23, Larval eighth abdominal and terminal segments (dorsal). 24, Same (ventral).

Larva. Third instar: Head directed an- as long as wide. Spatula (Figs. 18-20) with teriorly; cephalic apodemes stout, about as anterior tooth weakly to deeply emargin- long as head capsule. Antenna about twice ate apicomedially, the lobes rounded; shaft VOLUME 121, NUMBER 2 175 long, slender, parallel-sided, encroaching is due to both ground color of the wing second thoracic segment. Spiracles later- membrane and scales but, again, the ally disposed at midlength except eighth scales are easily lost and the mottling of abdominal spiracles situated at later- the membrane is usually faint. Although oposterior end of segment and directed the wing mottling appears to differ among posteriorly. Papillae as for basic plan of species, it is difficult to compare among Cecidomyiidi and Resseliella as outlined species without pristine specimens. in Mo¨hn (1955). Integument (Figs. 21-24) Claws of most known species are on dorsum smooth to nearly entirely peb- toothed on the foreclaws and simple on bled, second thoracic to seventh abdomi- the mid- and hindclaws. The few species nal segments with horizontal rows of tiny, known to have all the claws toothed are rounded spicules anteromedially, rows Resseliella piceae Seitner, Resseliella gradually more numerous from second kadsurae Yukawa, Sato & Xu, R. yagoi thoracic segment to seventh abdominal, and R. resinicola. The toothed foreclaws eighth abdominal and terminal segments of only the new species and Resseliella without spicules and mostly pebbled; clavula (Beutenmu¨ller) have an addi- venter pebbled or not as for dorsum, sec- tional smaller tooth (Fig. 6). ond thoracic to eighth abdominal seg- Male cerci are set at some remove ments with ventral anteromedial fields of from the hypoproct on Resseliella spe- spicules of two kinds, the more anterior cies, so slide preparations that flatten the rows rounded, posterior rows finer and terminalia skew them with regard to the pointed, except spicule rows of eighth hypoproct. Because of this, estimates of abdominal segment all rounded if present; cercal length with regard to that of the pleura pebbled. Terminal segment (Figs hypoproct can be inaccurate. In addition 23-24) dorsally partly to entirely pebbled the cerci do not appear to show specific with 6 short-setose papillae, one situated at differences. midlength of each of 2 prominent, conical, The protrusible distal half of the long usually pigmented, slightly dorsally re- ovipositor is not as stiff as in other curved, posterior lobes, each lobe termi- genera with long ovipositors, perhaps nating with corniform seta; ventral surface abetted by the absence of lateral scler- smooth to partly pebbled or spiculose, anal ites, so may show some accordioning. slit smooth or lined with pointed spicules, Although the structure does not lend perianal pads each bearing a single papilla itself to precise species measurement, its without seta, area posterior to perianal length compared to that of the seventh pads bearing 4 papillae without setae. tergite is still a useful species character. Remarks. At least half the known species were described as having one or Resseliella maxima Gagne´, more of banded antennae, banded legs new species and mottled wings. Antennal banding is urn:lsid:zoobank.org:act:4BF1A716- integumental but leg banding is due to 54A4-4C5F-92F1-B1391ED224D4 the color of the covering scales that are easily lost through handling and slide Adult. Color in life: Antenna (Fig. 3) preparation. Nevertheless, the pattern of with alternating ground color of dark and banding on the antennae and legs when it light bands; male with scape, pedicel, does occur is usually nearly entirely first flagellomere and first node and neck similar to that of the new species (Figs. of each successive flagellomere dark, the 2-3, 8-9). Mottling of the wing, however, remainder light, the female with basal 176 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON third of each node and neck dark, re- Remarks. This species is compared mainder light; wing (Fig. 2) mottled with here with two other species of Res- yellow and black scales reinforced by seliella, R. soya, which occurs on soy- light and dark ground color; legs (Figs. 8- bean in Japan, and R. clavula from 9) with alternating bands of dark and light Cornus florida (Cornaceae) in eastern scales, those on fore- and midlegs black North America, the only other species of except yellow at joint of femur and tibia, the genus known to share with the new on middle 1/3 of second tarsomere, basal species a second tooth on the foreclaws. 3/5 of third and fourth, and all of fifth; Resseliella soya is distinct from R. hindleg black except yellow on third 1/4 maxima in that its gonostylus (Fig. 15) is of femur, first and third 1/4 of femur, thinner and more strongly tapered, the basal 2/3 of second, third and fourth tar- gonocoxite has an obtuse mediobasal lobe, someres and all of fifth. Frons with 5-6 the protrusible part of the ovipositor, at setae on each side. Wing: length in males, about three times the length of the seventh 2.0-2.1 mm (n=4); in females, 2.3-2.5 tergite, is only half the length in R. max- mm (n=6). Anepimeron with 10-13 setae. ima, and the third instar differs in the more Claws (Figs. 6-7) anisomorphic, fore- deeply emarginate spatula tooth (Fig. 18). claws with two basal teeth, mid- and Differences are based on a male and two hindclaws untoothed. Male abdomen: females and six third instars from Oshiage, segments 6-8 as in Fig. 12; terminalia Hokuto City Hokkaido, Japan, as well as (Figs.13-14) with gonostylus evenly and thedescriptionandillustrationinYukawa only gradually tapered. Female abdomen (1971). Moreover, COI mitochondrial (Figs. 10-11): protrusible part of oviposi- gene segments of R. maxima are distinctly tor 5.9-6.5 times length sternite 7 (n=6). different from those of R. soya, showing Pupa. Unknown. an 8.5-8.7% pairwise distance. . Third instar: Orange in life. Resseliella clavula has a more strongly Spatula tooth (Fig. 20) slightly emar- tapered gonostylus (Fig. 16) and the gon- ginate. Thorax and first through seventh ocoxite is more bulbous than in either R. abdominal segments pebbled only on soya or R. maxima. The length of the pleura (Figs. 21-22). Eighth abdominal ovipositor is unknown. The tooth of the and terminal segments as in Figs. 23-24. third instar spatula is somewhat emargin- Material examined.—Holotype, male, ate and also noticeably erose (Fig. 19). reared from larva on soybean stem, Saun- This rough margin of the spatula tooth is ders, Nebraska, VII-7-2018, J. McMechan, apparent on all available third instars of R. deposited in USNM. Paratypes: same per- clavula.Thisspecieslivesinawoodygall, tinent data as holotype, 4 males, 8 females, which may possibly explain the uneven larvae, all deposited in USNM except 1 margin. These observations are based on male, 1 female and 4 larvae deposited in two males from Albany, NY, one male Entomological Laboratory, Kyushu Uni- from Stamford CT, two third instars from versity, Fukuoka, Japan. Other specimens, Hewitt, NJ, ten third instars from Richmond deposited in USNM: 10 larvae, Griswold, Hill, GA, and two third instars from Iowa, IX-2018, Michael Leetch; 10 larvae, Gainesville, FL. VIII-2018, Iowa, Jessie Alt. Etymology.—The name maxima means ACKNOWLEDGMENTS greatest, reflecting both the insect’s po- tential importance to soybean and the We thank Dr. Jung Wook (“Woogie”) host’s name, G. max. Kim, USDA-APHIS-PPQ-PHP, National VOLUME 121, NUMBER 2 177

Identification Services, for the final ar- of phytophagous beetles (Chrysomelidae: rangement and labelling of the plates; Opharaella). Molecular Biology and Evolution Dr. Y. Nagano, Analytical Center for 12: 627–640. Gagne´, R.J. 1989. The Plant-Feeding Gall Experimental Sciences, Saga University, Midges of North America. Cornell University for his careful assistance with the molec- Press, Ithaca, New York. xi & 356 pp. ular analysis; Mr. Motohiko Aoki, Local Gagne´ 2018. Key to Adults of North American Independent Administrative Agency Hok- Genera of the Subfamily Cecidomyiinae kaido Research Organization, Donan Ag- (Diptera: Cecidomyiidae). Zootaxa 4392: ricultural Experiment Station, Hokkaido 401-457. Gagne´, R.J. and M. Jaschhof. 2017. A Catalog of 041-1201, Japan for his recent collections Cecidomyiidae of the World. 4th Edition. Digital. of R. soya from Hokkaido; Mike Leetch, 762 pp. https://www.ars.usda.gov/ARSUserFiles/ Syngenta, Des Moines, IA, and Jessie Alt, 80420580/Gagne_2017_World_Cat_4th_ed. Corteva Agrisciences, Dallas Center, IA, pdf. USA for larval specimens; and journal re- Kolesik, P. and G. Baker. 2013. New species of viewers Netta Dorchin, Tel Aviv Univer- Resseliella (Diptera: Cecidomyiidae), inju- rious to Dianella and Phormium (Xanthor- sity, Israel, and Peter Kolesik, Adelaide, rhoeaceae) in Australia and New Zealand. SA, Australia, for their careful reading and Australian Journal of Entomology 52: 67– comments on the manuscript. 72. Mention of trade names or commercial Mo¨hn, E. 1955. Beitra¨ge zur Systematik der products in this publication is solely for Larven der Itonididae (=Cecidomyiidae, the purpose of providing specific in- Diptera). 1. Teil: und Itoni- dinae Mitteleuropas. Zoologica 105 (1&2): formation and does not imply recom- 1–247, 30 pls. mendation or endorsement by the USDA. Simon C., F. Frati, A. Beckenbach, B. Crespi, H. USDA is an equal opportunity provider Liu and P. Flook (1994) Evolution, weight- and employer. ing, and phylogenetic utility of mitochondrial gene sequences and a compilation of con- Literature Cited served polymerase chain reaction primers. Annals of the Entomological Society of Elsayed, A.K, K. Ogata, K. Kaburagi, J. America 87: 651–701. Yukawa and M. Tokuda (2017) A new Da- Tamura, K., Stecher, G., Peterson, D., Filipski, sineura species (Diptera: Cecidomyiidae) A., and Kumar, S. 2013. MEGA6: molecular associated with Symplocos cochinchinensis evolutionary genetics analysis version 6.0. (Loureiro) (Symplocaceae) in Japan. Japa- Molecular Biology and Evolution, 30: 2725– nese Journal of Systematic Entomology 23: 2729. 81–86. Yukawa, J. 1971. A revision of the Japanese gall Funk D.J., D.J. Futuyma, G. Orti and A. Meyer midges (Diptera: Cecidomyiidae). Memoirs (1995) Mitochondrial DNA sequences of the Faculty of Agriculture, Kagoshima and multiple data sets: a phylogenetic study University 8: 1–203.