PROC. ENTOMOL. SOC. WASH. 108(4), 2006, pp. 985-994 DETECTION AND ESTABLISHMENT OF THE EUROPEAN CRANE FLIES TIPULA PALUDOSA MEIGEN AND TIPULA OLERACEA L. (DIPTERA: TIPULIDAE) IN NEW YORK: A REVIEW OF THEIR DISTRIBUTION, INVASION HISTORY, BIOLOGY, AND RECOGNITION DANIEL C. Peck, E. RICHARD HOEBEKE, AND CAROLYN KLASS (DCP) Department of Entomology, NYSAES, Cornell University, 630 W. North St., Geneva, NY 14456, U.S.A. (e-mail: [email protected]); (ERH, CK) Department of Entomology, Comstock Hall, Cornell University, Ithaca, NY 14853-2601, U.S.A. (e-mail: [email protected]; [email protected]) Abstract.4Two species of European crane flies are newly documented from New York based on collections from several localities during the period 2004 to 2006. Larvae of Tipula paludosa Meigen and T. oleracea L. are injurious to turf and pasture grasses and certain other crops in areas of previous establishment, such as British Columbia and the Pacific Northwest (both species) and Ontario and Quebec (7. paludosa). Initial observations on their association with turfgrass in New York are summarized along with background information on their invasion history, biology, and pest status. Known collection records are listed and mapped for both species. Recognition features are discussed and photographic illustrations of key morpho- logical features are provided to aid their differentiation from native and non- injurious crane flies and from each other. Key Words: European crane flies, Tipula paludosa, Tipula oleracea, invasive species, turfgrass pests, leatherjackets Crane flies belonging to the subgenus North America, biology, pest status, Tipula (Tipula) are principally Palearctic and recognition features. and Ethiopian in their distribution. No indigenous species of the subgenus 77- DETECTION EVENTS IN NEw YORK pula have been recorded in the New In the summer of 2004, extension World. Current evidence suggests that 7. agents of Cornell Cooperative Extension paludosa Meigen has established in three (CCE) channeled reports to us that led disjunct geographic regions of North to the discovery and confirmation of America, while 7: oleracea L. has colo- T. paludosa and T. oleracea in extreme nized in two regions of North America northwestern NY. In late June, grounds and one in South America. Herein we personnel of the Niagara County Golf give the circumstances surrounding the Club in Lockport, NY noticed large initial discovery of both species in New numbers of crane flies emerging from York in 2004, and also summarize in- the turf. They found pupal cases first, formation from the literature on their and shortly thereafter adults were dis- invasion history and distribution in covered. Some exuviae were collected, 986 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON initially submitted to CCE Niagara Co., tytipula) paterifera Alexander, and T. and then directed to the Cornell Univer- (Platytipula) ultima Alexander. sity Insect Diagnostic Laboratory for identification. Because a species identifi- DISTRIBUTION AND INVASION HIstTory cation could not be provided based on Tipula paludosa is a native of the West the pupal exuviae alone, adults were Palearctic Region and is an important collected and sent directly to Cornell. pest in grasslands in areas with an The adult specimens were positively Atlantic climate (Darvas et al. 2000). identified. (by WERE) as= one9 vof=<the It is referred to as the 8marsh crane fly9 European crane flies, Tipula oleracea. in Europe and more commonly as the By August 2004, word of this detection 8European crane fly9 in North America. had spread and other golf course super- In western North America, this species intendents were on the lookout for the occurs in the Pacific Northwest where it presence of unusually large numbers of ranges from southern British Columbia, crane flies. At the Niagara Falls Country western Washington and Oregon to as Club in Lewiston, NY the superinten- far south as northern California (Wil- dent collected a series of crane flies for liams et al. 1989, Umble and Rao 2004, identification because large numbers Rao et al. 2006). It is largely limited to were Observed emerging from the rough regions west of the Cascades with some areas of the turf. Interestingly enough, isolated infestations in central Washing- ton. In eastern North America, it is these, crane flies: <were identified= (by reported from the provinces of New- ERH) as yet another European species, foundland, Nova Scotia, Ontario and Tipula paludosa. These records are the first for both species in the Northeast Quebee (Simard Yer" al) int press) elias unknown whether the Ontario popula- United States. tion is continuous with the other eastern Both species were listed as primary provinces. targets for the national Cooperative Tipula paludosa was inadvertently in- Agricultural Pest Survey (CAPS) pro- troduced into Newfoundland as early as gram in 2004 and 2005 before being 1880 (Alexander 1962) and was detected unlisted in 2006. After these initial finds, in northern Nova Scotia (Cape Breton horticultural inspectors for the NYS Island) in 1955 (Fox 1957, Beirne 1971). Department of Agriculture and Markets The species was later detected in 1965 on continued to collect crane flies from the the western coast in British Columbia two original sites and from surrounding (Wilkinson and MacCarthy 1967) and areas. As a result, other collections of T. a year later in Washington (Jackson and paludosa in Erie Co. and Niagara Co. Campbello 1975): In *Ontario} ats aiinst were confirmed in 2004: in the town of definitive identification was in 1998, but Amherst (two residential sites), and from crane fly damage reported in 1996 and two state parks (Four Mile Creek and 1997 suggests an earlier establishment Goat Island) in the Niagara Falls area. (Charbonneau and Dupuis 1999). This Several native species (determined by species9 appearance in northwestern New J. K. Gelhaus, Academy of Natural York was probably inevitable given it is Sciences, Philadelphia, PA) were also widespread throughout southern Ontario collected in abundance at the same sites including the areas of Ancaster, Hamil- in Lockport and Lewiston, including ton, Niagara Falls, Toronto and Whitby Tipula (Beringotipula) borealis Walker, (Charbonneau and Dupuis 1999). T. ( Yamatotipula) furca Walker, T. Tipula oleracea is a native of the West ( Yamatotipula) sayi Alexander, T. ( Pla- Palearctic Region and northern Africa VOLUME 108, NUMBER 4 987 1 Tipula paludosa 2 Tipula oleracea gNiagaara Co. t! Monroe Co. Ni? agara Co. Monroe Co. Oswegpo yC o. 3 e ®e mt) oe as e Nassau Co e Figs. 1-2. New York localities where European crane flies were detected in 2004-2006. 1, Tipula paludosa. 2, T. oleracea. (Oosterbroek and Theowald 1992). In from Farmington, Michigan, a Detroit central Europe, it is the most frequently suburb (Gelhaus 2006). encountered crane fly species (Darvas et It is very likely that the introductions alee2000): and is referred: to as the of both species were due to movement of 8common9 or 8cabbage9 crane fly. In infested soil media, meaning that ship- North America, it has been variously ments of sod and container stock could referred to as the 8(giant) common9 or occasion their spread locally and re- 8marsh9 crane fly. In western North gionally. It is unclear whether the popu- America, this species occurs 1n southern lations in Ontario and New York repre- British Columbia, western Washington sent direct introductions from Europe, or and Oregon, and as far south as northern secondary introductions from other re- California (LaGasa and Antonelli 2000, gions of North America where they have Umble and Rao 2004, Rao et al. 2006). been previously established. Although considered a more recent in- Material examined.4Voucher speci- troduction to the Pacific Northwest, its mens (all adults) of the two species from widespread distribution suggests it may the following localities in New York are have gone undetected for a number of deposited in the Cornell University In- years (Umble and Rao 2004). sect) (Collection <(lthacay SNIY)~ *ibese Tipula oleracea was first reported on localities are mapped in Figs. 1-2. the North American continent in British Tipula paludosa Meigen (Fig. 1).4 Columbia (Vancouver) in 1998 (Costello UNITED STATES: New York: Erie 1998). Surveys in the Pacific Northwest Co., Amherst (two residential sites), 14 for adults in 1999 and 2000 indicated the September 2004, W. Eilsworth. Monroe presence of T. oleracea throughout west- Co., Penfield (Penfield Country Club), 3 ern Washington and in the northern October 2005, R. Ferrentino; Pittsford Willamette Valley of western Oregon (Locust Hill Country Club), 4 September (LaGasa and Antonelli 1999, Umble 2005, D. C. Peck; Pittsford (two residen- and Rao 2004). It was detected in 1999 tial sites): 121 September 20054 Die: in Andean Ecuador (South America) Peck: 27)September 2005, Wines Peekart (Young et al. 1999). In May 2005, T. November 2005, D. C. Peck; Rochester oleracea was identified and reported (Irondequoit Country Club), 15 Novem- 988 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON ber 2005; DD; <Gy Peck= Niagara. Go:. day (7. paludosa) or 3-4 days (T. oler- Lewiston (Niagara Falls Country Club), acea) of their brief reproductive lives, 1 September 2004, E. R. Hoebeke & C. either in a single batch because gravid Klass: )2 1) Septembere2005 51D. -C Beck: females are unable to fly any distance Lockport (Willowbrook Golf Course), (T. paludosa) or in_ several batches 21 September 2005, D. C. Peck; Niagara because gravid females are more capable Falls. (Hyde. Park..Golf Course); 21 fliers (7. oleracea). Each will deposit September 2005, D. C. Peck; Niagara 200-300 black eggs at or near the soil Falls (Goat Island State Park), 9 Sep- surface, hatching in 1.542 (T. paludosa) tember 2004, W. Ellsworth; Youngstown or | (T. oleracea) weeks. The thick- (Four Mile Island State Park), 9 Sep- skinned larvae are commonly known as tember 2004, W. Ellsworth. leatherjackets; these will develop through Tipula oleracea L. (Fig. 2)4UNITED four instars and reach 3-4 cm in length STATES: New York: Monroe Co., Pitts- before pupation. Larvae mostly inhabit ford (Locust Hill Country Club), 4 the top 3 cm of the soil where they feed September 2005, Ds C. Peck: Nassau on the roots, root hairs, crowns and Co., New Hyde Park, 24-30 April 2006, blades of turfgrass. On warm humid N. Lolis, on outside of house. Niagara nights, larger larvae may emerge to Co., Lockport (Niagara County Golf forage on stems and grass blades on the Course), 24 June 2004, K. Kreppenneck; soil surface. The most salient difference 1 July 2004, E. R. Hoebeke & C. Klass; between the two species is that T. 1 September 2004, E. R. Hoebeke & paludosa is univoltine, with adult emer- @. Klass; 9-June 2005) BP R.. <Hoebeke & gence in the fall. Larvae overwinter as C. Klass; Lockport (Willowbrook Golf third instars, develop through fourth Course), 9 June 2005, E. R. Hoebeke & C. instars in the spring, and by early June Klass; Youngstown (Niagara Frontier will move 345 cm deep in the soil where Golf Club), 9 June 2005, E. R. Hoebeke they remain in a non-feeding stage for 64 & C. Klass. Oswego Co., Fulton (Battle 8 weeks until pupation. In contrast, 7. Island Golf Club), | September 2005, D. oleracea is bivoltine with adult emer- @yePecks 24) September 2005,) EvakR: gence in both spring and fall. This Hoebeke. species lacks a long aestivation stage. BIONOMICS DAMAGE AND PEstT STATUS The biology of both species is included The impact and management of 7. in reviews by Wilkinson and MacCarthy paludosa and T. oleracea are reviewed (1967), Jackson and Campbell (1975), and summarized in Wilkinson and Mac- and Blackshaw and Coll (1999), as well Carthy (1967) and Blackshaw and Coll as a review of the family Tipulidae by (1999). All turf and forage grass species Pritchard (1983). As summarized here appear to be acceptable hosts for larvae from the literature, many aspects of the (Pesho et al. 1981). West of the Cascades, biology of 7. paludosa and T. oleracea they are regarded as the most serious are similar. Mature pupae wriggle to the insect pests in lawns, pastures and hay soil surface so the adult fly can emerge. fields (see: http://www.puyallup.wsu.edu/turf/ On low mown turf, like golf course tees research/cranefly.htm). Although problem- and putting greens, the pupal exuviae atic in any type of turfgrass management look like black twigs poking up from the system, they are dependent on moist soil surface where they can be readily de- conditions and according to. studies tected. Adult females will emerge, mate conducted in Europe, survival is favored and lay most of their eggs within the first by mild winters and wet, cool summers VOLUME 108, NUMBER 4 989 (Maercks 1941, cited by Wilkinson and MacCarthy 1967). In addition to grasses, leatherjackets have the potential to affect cereal and other crops in North America. In British Columbia they are serious pests in seedling nurseries, af- fecting transplant bare root stock, but also container stock where they girdle the stem at the soil line (Sutherland et al. 1989). In Oregon, they have become problematic in cultivated peppermint (Rao and Gelhaus 2003) and grass seed fields (Rao et al. 2001) and are linked to damage in winter wheat and turnips (S. Rao, personal communication). In their endemic European range, they are in- jurious pests of winter and spring cereals ig, 3 Wing base of Tipula paludosa, showing and can become troublesome in a variety squamal hairs (arrow). of minor crops ranging from flowers, crucifers and brassicas to sugar beets, on the Mississippi Gulf Coast (Held and carrots and berries (Blackshaw and Coll Gelhaus 2006). 1999): FIELD OBSERVATIONS IN NEw YORK One study in the northwest U.S. estimated that 46% of homeowners in The relative abundance, habits, and western Washington treated for leather- host preferences of both 7: paludosa and jackets at an estimated annual cost of T. oleracea were documented by DCP in $12.9 million for homeowner applied 2004, based on personal observations at treatments (LaGasa and = Antonelli two golf course sites in northwestern 2000). Economic damage estimates from New York and on personal communica- Europe portend the potential threat of tions from golf course personnel of these leatherjackets to regions in the U.S. facilities. Despite some anecdotal obser- where they become established. For vations, no visual damage to turf could instance, studies from Northern Ireland be definitively associated with the pres- estimated leatherjacket damage to forage ence of larvae. These field observations grasses at >£15 million each year, with are summarized below. yield increases of 74% after control of Lewiston (Niagara Co.).4Populations larvae (Blackshaw 1994). of JT. paludosa were widespread and Of over 1600 species of crane flies abundant at the Niagara Falls Country reported for the U.S., few others are Club. In spring 2004, the golf course linked to agricultural damage. Two superintendent estimated some _ larval contemporary grass pests are Tipula populations to be on the order of 304 simplex Doane and Tipula umbrosa Loew 40/ft- in the rough, possibly associated (Beckwiandijieldantspress)iirlhe srange with sparse damage (K. Holthouse, crane fly, 7. simplex, is a pest of non- personal communication). Those popu- irrigated pastureland throughout central lation levels fell well within suggested California (Hartman and Hynes 1977), economic control thresholds that range while 7. umbrosa has been recently widely from 15440/ft9 (Campbell 1975, reported as damaging in centipede grass Charbonneau and Dupuis 1999). The (Eremochloa ophiuroides [Munro] Hack.) superintendent reported seeing fall pop- 990 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON 4 errs STE ks The TSE SLITS OF VF SSI erwe n Figs. 4-5. Wing of Tipula oleracea, illustrating darker area and whitish stripe along the leading (costal) margin. 1, With light background. 2, With dark background. ulations of adult crane flies from 2001 to flitting about low over the grass and in 2003, suggesting the possibility that they copula, Another visit was made on 11 were established as much as three years October 2004. Despite being so late in prior to their first confirmation. No the season, a live larva and a few adults adult emergence in the spring associated were still observed. A broader survey of with the presence of 7. oleracea was crane fly incidence across the course noted. Crane fly larval habitat at this site showed that pupal exuviae or adults included perennial ryegrass (Lolium per- were still detected on 100% of holes enne L.), Kentucky bluegrass (Poa pra- (n = 13), 70% of tees (n = 37) and 56% tensis L.), annual bluegrass (Poa annua of the greens (n = 9) that were sampled. L.) and tall fescue (Festuca rubra L.). Lockport (Niagara Co.).4At this site, During a visit on 9 September 2004, populations of 7. oleracea were relatively hundreds of dead and dying adults were sparse. Starting mid May, the superin- found clinging to the tips of branches on tendent reported seeing abundant (<<hun- a hedgerow which bordered roughs dreds of99) pupae and low-flying adults along the length of two fairways where around one green and one tee in partic- infestations were greatest. Live pupae ular that bordered a stream and woods and pupal exuviae were seen on various (K. Kreppenneck, personal communica- tees and greens. Active adults were seen tion). He described visible damage in the VOLUME 108, NUMBER 4 991 form of scalping and discoloration of the several morphological features (Coe et grass in a <1-inch diameter area around al. 1950, Den Hollander 1975, LaGasa some of the spots where the pupal 2000). Ventral spacing between the eyes exuviae emerged. He noticed exuviae at is two or more times the width of the a few other greens on the course as well, scape in 7. paludosa (Fig. 6), whereas it including the practice green near the is much narrower in 7. oleracea, at most clubhouse. Crane fly larval habitat at equal to the width of the scape (Fig. 7). this site included P. annua, P. pratensis There are 14 antennal segments in 7: and creeping bentgrass (Agrostis stoloni- paludosa compared to 13 in 7. oleracea. ferat2). The eye and antennal characters apply to During a visit on 28 June 2004, soil both males and females. An additional core sampling on the green where the character for females is wing to abdom- original infestation occurred did not inal length ratio. Wings of female 7. yield any specimens in addition to those paludosa are shorter than the abdomen sent previously by the golf course. On | (Fig. 8), while wings of female 7. o/er- July 2004, no specimens were found after acea are Clearly longer than the abdomen extensive scouting with soap drenches to (Fis9)s Ini <the (case (of maales; cathe flush larvae, soil cores to dig for larvae, genitalic characters are quite distinct and visual searches for pupal exuviae. between the two species as illustrated in Sweep net samples from the surrounding Figs. 10-11. woods and vegetation, however, yielded There are no reliable morphological one additional 7. oleracea female. characters for separating larvae of T. paludosa and T. oleracea from each RECOGNITION FEATURES other. Although the anal papillae of Adults of Tipula paludosa and_ T. larvae are dimorphic (Brindle 1960), this oleracea are almost identical in appear- character is not robust enough to be ance with grayish-brown bodies. Adults diagnostic (Humphreys et al. 1993). The are 1.542.5 cm long (not including legs), only confident means of identifying pupae 3.043.5 cm, mature larvae 3-4 cm, larvae is to rear them to adult. Neverthe- and eggs 0.1 cm. Among some common less, larvae of the subgenus Tipula native species of 7ipu/a occurring in the (Tipula) (including paludosa, oleracea) same habitats (lawns and wet pastures), can be separated from other North adults of these two exotic species can be American Tipula by referring to the recognized by the wing base with a patch larval key presented in Gelhaus (1986). of short, but distinct, squamal hairs A recent study has shown that mito- (Fig. 3) (Alexander and Byers 1981). chondrial DNA cytB sequencing is an Another distinguishing feature of these accurate method for separating the immigrant crane flies is that the leading larvae and adults of 7. paludosa and T. edge of the wing is bordered by a narrow oleracea from each other and from native smoky band adjacent to a whitish band. species (Rao et al. 2006). Also, Brindle This feature is best observed against (1960) listed features useful for distin- a light- and dark-colored background, guishing pupae of the two species. respectively (Figs. 4-5). Unlike many ACKNOWLEDGMENTS other native species, there are no pig- mented areas on the veins or cross-veins We thank Brian Eshenaur (Cornell and no other spots or <8pictures=9 on the Cooperative Extension, Monroe Co.), wings. John Farfaglia (Cornell Cooperative Adults of both species can be reliably Extension, Niagara Co.), Khlar Holt- differentiated from each other based on house (Niagara Falls Country Club, 992 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON Figs. 6-11. Diagnostic characters for separating the European crane flies Tipula paludosa and T. oleracea. 647, Ventral surface of head illustrating compound eye separation. 6, 7. paludosa. 7, T. oleracea. 8-9, Wing length compared to abdominal length (females only). 8, Wings shorter than abdomen (7. paludosa). 9, Wings longer than abdomen (T. oleracea). 10-11, Male genitalia (left inner gonostylus, dorsal aspect). 10, 7. paludosa. 11, T. oleracea. (Note: In intact male specimens, the large, flap-like outer gonostylus conceals most of the inner gonostylus; to properly examine the inner gonostylus, the outer gonostylus must be moved or removed.) VOLUME 108, NUMBER 4 993 Lewiston, NY) and Kevin Kreppenneck the view of the U.S. Department of (Niagara County Golf Course, Lock- Agriculture. port, NY) for alerting us to initial populations of European crane flies: LITERATURE CITED Pam Charbonneau (Guelph Turfgrass Alexander, C. P. 1962. Taxonomic studies of crane Institute, Guelph, Ontario) and Anne flies of Newfoundland. Year Book of the American Philosophical Society, pp. 267-271. Schattmann (Weed Man, Niagara Re- Alexander, (©. JP and 1G. We Byerss 19815 7: gion, Ontario) for showing us infesta- Tipulidae, pp. 153-190. In McAlpine, J. F., tions in Ontario; Jon Gelhaus (Dept. of B. V. Peterson, G. E. Shewell, H. J. Teskey, J. Entomology, The Academy of Natural R. Vockeroth, and D. M. Woods, eds. Manual Sciences, Philadelphia, PA) for confirm- of Nearctic Diptera, Vol. 1. Research Branch, Agriculture Canada, Monograph No. 27. ing the initial identification of 7. palu- Beirne, B. P. 1971. Pest insects of annual crop dosa, for identifying native species col- plants in Canada. Memoirs of the Entomolog- lected in association with these exotic ical Society of Canada 78: 1-124. species, and for numerous suggestions Blackshaw, R. P. 1994. Sampling for leatherjackets which improved this paper: Kennoth in grassland. Aspects of Applied Biology 37: 95-102. Carnes (NYS Dept. of Agriculture & Blackshaw, R. P. and C. Coll. 1999. Economically Markets, Albany, NY) and William important leatherjackets of grassland and Ellsworth (NYS Dept. of Agriculture & cereals: Biology, impact and control. Integrat- Markets, Amherst, NY) for sharing in- ed Pest Management Reviews 4: 143-160. formation managed by the NYS CAPS Brindle, A. 1960. The larvae and pupae of the British Tipulinae (Dipt., Tipulidae). Transac- program; Anuar Morales and Maria tions of the Society for British Entomology 14: Diaz (Dept. of Entomology, NYSAES, 63-114. Cornell University, Geneva) for assis- Campbell, R. L. 1975. Insecticidal control of tance in the field; Eric LaGasa (Wash- European crane fly in Washington. Journal ington Dept. of Agriculture, Olympia, of Economic Entomology 68: 386-388. Charbonneau, P. and J. Dupuis. 1999. Report on WA) for providing wing photographs of Tipula paludosa in Ontario, 1999. 1999 Annual T. oleracea; Daniel Olmstead for con- Research Report, Guelph Turfgrass Institute, structing the distribution maps (Dept. pp. 153-156. of Entomology, NYSAES, Cornell Uni- Coe, R. L., P. Freeman, and P. F. Mattingly. 1950. versity, Geneva); and Kent Loeffler Diptera: Nematocera. Families Tipulidae to Chironomidae. Handbooks for the Identifica- (Dept. of Plant Pathology, Cornell Uni- tion of British Insects. 9, Part 2. versity) for providing assistance with Costello, B. 1998. 1998 Crop protection newsletter. the photography and arrangement of B.C. Ministry of Agriculture and Food, figures. Vol. 20 No. 2. Plant Industry Branch, Crop Protection Program, Kelowna, BC, Canada. This research was supported, in part, by Darvas, B., M. Skuhrava, and A. Andersen. 2000. the New York State Agricultural Exper- Agricultural dipteran pests of the Palearctic iment Station federal formula funds, Pro- region, pp. 565-649. In Papp, L. and B. ject No. NYG-621508 to DCP; by the Darvas, eds. Contributions to a Manual of Cornell University Agricultural Experi- Palearctic Diptera, Vol. | (General and Ap- plied Dipterology). Science Herald, Budapest. ment Station federal formula funds, Pro- Den Hollander, J. 1975. The phenology and ject No. NYC-139413 to ERH, received habitat of the species of the subgenus Tipula from Cooperative State Research, Educa- Linnaeus in the Netherlands (Diptera, Tipuli- tion, and Extension Service, U.S. De- dae). Tijdschrift voor Entomologie 118: 83497. partment of Agriculture; and by the NYS Fox, C. J. S. 1967. Note on occurrence in Cape Breton Island of Tipula paludosa Mg. (Diptera: CAPS funds to CK. Any opinions, find- Tipulidae). Canadian Entomologist 89: 288. ings, conclusions, or recommendations Gelhaus, J. 1986. 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