Table Of ContentPROC. ENTOMOL. SOC. WASH.
98(1), 1996, pp. 93-99
ESTABLISHMENT OF UROPHORA AFFINIS ON SPOTTED KNAPWEED IN
PENNSYLVANIA, WITH NEW EASTERN U.S. RECORDS OF
U. QUADRIFASCIATA (DIPTERA: TEPHRITIDAE)
A. G. WHEELER, JR. AND CRAIG A. STOOPS
Bureau of Plant Industry, Pennsylvania Department of Agriculture, Harrisburg, PA
17110, U.S.A.; (CAS) Present address: Department of Entomology, Clemson University,
Clemson, SC 29634, U.S.A.
Abstract.(cid:8212)The Old World tephritid Urophora affinis (Frauenfeld) is a gall-inducing
seedhead fly released in western and eastern North America for the biological control of
knapweeds, Centaurea spp. (Asteraceae). Its establishment and spread in the West are
well documented, but recoveries in the East have been few: in New York near release
sites in Essex and Warren counties and at unspecified localities in Quebec and Virginia
(presumably at or near release sites). Urophora affinis is reported as a new state record
from Pennsylvania (7 counties), and its establishment in central New York State is re-
corded. Urophora quadrifasciata (Meigen), another Palearctic species introduced for
knapweed control, is recorded for the first time from Maryland, Virginia, and West Vir-
ginia, and its known range in Pennsylvania is extended.
Key Words: Insecta, Tephritidae, seedhead flies, distribution, spotted knapweed, biolog-
ical control
The tephritid genus Urophora includes ican authors) (Harris and Myers 1984,
about 100 species whose larvae are nearly Miiller et al. 1988, Kartesz 1994). Spotted
always associated with plants of the Aster- knapweed is also common in the Northeast
aceae. Eight species are indigenous to the (USDA 1971, Gleason and Cronquist
Nearctic Region, and three Eurasian spe- 1991).
cies(cid:8212)U. affinis (Frauenfeld), U. quadrifas- Urophora affinis and U. quadrifasciata
ciata (Meigen), and U. sirunaseva (Her- are seedhead flies whose larvae feed in
ing)(cid:8212)have been introduced to North Amer- buds and in flower heads of their herba-
ica for the biological control of adventive ceous hosts, with females of U. affinis ovi-
knapweeds, Centaurea spp. (White and positing in smaller heads than those of U.
Korneyev 1989, Turner et al. 1994). Several quadrifasciata. Larvae of the two species
members of this composite genus infest are able to coexist in capitula of their hosts
rangelands and pastures in western North (Berube 1980, Harris 1980a, Shorthouse
America (Watson and Renney 1974, Mad- 1990). The mostly univoltine U. affinis in-
dox 1979, Strang et al. 1979, Harris and duces a complex gall from tissues of the
Myers 1984, Miiller-Scharer and Schroeder ovary and receptacle; the thinner, more sim-
1993). The most economically important ple gall of U. quadrifasciata, a predomi-
Species in the West are diffuse knapweed, nantly bivoltine species, is restricted to tis-
C. diffusa Lam., and spotted knapweed, C. sues of the ovary wall (Shorthouse 1978a,
biebersteinii DC. (= C. maculosa of Amer- b, 1990, Story et al. 1992). Galls of U. af-
94 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
finis are greater energy sinks than those of tablishment in central New York, and spec-
U. quadrifasciata, reducing seed production ulate on the origin of these populations. We
even in uninfested capitula (Harris 1980b, also provide the first records of U. quadri-
Myers and Harris 1980, Shorthouse 1990). fasciata from Maryland, Virginia, and West
Despite negative interaction between these Virginia, and extend its previously recorded
biological control agents, their effects on distribution in Pennsylvania.
host plants are complementary, and knap-
METHODS
weed seed is reduced more in areas where
the flies coexist (Berube 1980, Harris Urophora affinis.(cid:8212)The first Pennsylva-
1980b, Myers and Harris 1980, Harris and nia specimens were collected at Tamaqua
Myers 1984). (Schuylkill Co.), Pa., on 23 June 1994. In
Following initial releases of both tephri- late June we began surveying spotted knap-
tids in British Columbia in the early 1970s, weed colonies observed within 50-60 km
their establishment in that province and the of the detection site in an attempt to delimit
western United States (Washington to Cal- the fly(cid:8217)s distribution in eastern Pennsylva-
ifornia plus Idaho and Montana) has been nia. Capitula of knapweed growing on sha-
well documented (Maddox 1979, 1982, ly roadside banks, in road maintenance or
Harris and Myers 1984, Story et al. 1987, construction spoils, along railroad rights-of-
Julien 1992, Foote et al. 1993, Hoebeke way, in urban vacant lots, and in other dis-
1993, Miiller-Scharer and Schroeder 1993). turbed sites were swept with a standard in-
They were also released in eastern North sect net. The number of sweeps varied with
America: U. affinis in Ontario (1970-1971), colony size but usually consisted of at least
Quebec (1979-1980), Maryland, New York several hundred. Any U. affinis adults ob-
(1983), and Virginia (1985-1986); and U. served were collected for laboratory veri-
quadrifasciata in Quebec (1979), Mary- fication of tentative field identifications.
land, and New York (1983) (Harris and Our surveys apparently were initiated be-
Myers 1984, Julien 1992, Hoebeke 1993). fore adult populations had begun to decline,
Postrelease monitoring in the East, howev- based on the presence of greater numbers
er, has been less thorough than in western of males than females, or at least about
North America. Not until the early 1990s equal numbers of both sexes; males tend to
was the eastern establishment of either spe- emerge earlier (Story and Anderson 1978).
cies reported. Based on surveys during Surveys continued until late August, al-
1990 to 1992 (Hoebeke 1993), U. quadri- though no adults were seen after mid-July.
fasciata was found to be widespread from Similar, but less extensive, sampling of
New England (Connecticut, Massachusetts, knapweed was conducted in 1994 in north-
New Hampshire, Rhode Island, and Ver- central Pennsylvania (A.G.W., C.A.S.) and
mont) south to New York, New Jersey, and in central and south-central New York (E.
Pennsylvania. No specimens of U. affinis, R. Hoebeke, A.G.W.). In 1995, additional
however, were collected from Centaurea delimiting surveys were made in eastern
spp. during surveys for U. quadrifasciata Pennsylvania (A.G.W.).
in the Northeast, although recoveries had Urophora quadrifasciata.(cid:8212)Spotted knap-
been reported at release sites in Essex and weed was sampled during 1994-1995 in
Warren counties, N.Y., in 1985 (Foote et al. portions of Maryland, Virginia, and West
1993, Hoebeke 1993). The only other east- Virginia(cid:8212)states from which this tephritid(cid:8217)s
ern records of U. affinis are Quebec and establishment had not been previously re-
Virginia, cited without specific localities by corded. Limited sampling was also con-
Julien (1992). ducted in several western Pennsylvania
Here we give the first records of U. af- counties where this species had not been
finis from Pennsylvania, document its es- found in earlier surveys (Hoebeke 1993).
VOLUME 98, NUMBER 1
Urophora affinis
© Detection sites
© Negative sites
(s mn
ee tore
Known distribution of Urophora affinis in New York and Pennsylvania. Shading indicates counties
in which biological control releases were made; release sites in eastern Canada, Maryland, and Virginia are not
shown.
Voucher specimens of both species have 1995) from Centaurea biebersteinii. New
been deposited in the Cornell University In- York collections were made in 1994 by E.
sect Collection, Ithaca, NY (CUIC) and R. Hoebeke from the same plant species.
Pennsylvania Department of Agriculture In- NEW YORK: Cortland Co., Cortland-
sect Collection (PADA); specimens of U. ville, 2 July; Seneca Co., 1 mi. N. of Inter-
affinis have been deposited at the National laken, 3 July; Tompkins Co., Dryden, Ith-
Museum of Natural History, Washington, aca, and Taughannock Falls State Park, 2(cid:8212)
DC (USNM). 4 July. PENNSYLVANIA: Berks Co.,
Hamburg, 5 July; Carbon Co., Bowmans-
RESULTS
town, 11 July; Jim Thorpe, 23 June; Colum-
Urophora affinis.(cid:8212)The following re- bia Co., Aristes, Centralia, and 6 mi. S. of
cords, representing the first for Pennsylva- Numidia, | July; Lehigh Co., Jacksonville,
nia and first for New York except recover- New Tripoli, 5 July; Luzerne Co., Rt. 81 nr.
ies at release sites in the Adirondacks, ex- Dorrance exit, 30 June; Hazleton, 23 June;
tend the known distribution of U. affinis in Nescopeck, 27 June; Northumberland Co.,
eastern North America (Fig. 1). All Penn- Coal Twp. N. of Shamokin, 13 June; Mount
sylvania collections were made by the au- Carmel, 6 July; Schuylkill Co., NE. of
thors in 1994 (except Northumberland Co., Barnesville, 30 June; Frackville, 23 June;
96 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
Frey
Fig. 2. New records of Urophora quadrifasciata in eastern United States.
Hegins, 29 June; Llewellyn, 7 July; N. of Covington, 26 June; Appomattox Co., Rt.
Mahanoy City, 27 June; New Ringgold, 5 460, Spout Springs, 3 July; Augusta Co.,
July; Pottsville, 7 July; Tamaqua, 23 June, Staunton, 25 June; Waynesboro, 3 July;
7 July; Rt. 209 N. of Tamaqua, 23 June; Bath Co., Rt. 39 E. of Millboro Springs, 3
Tremont, 7 July. July; Bedford Co., Bedford, 3 July; Buck-
Urophora quadrifasciata.(cid:8212)The known ingham Co., Sprouses Corner, 4 July;
eastern distribution is extended to include Campbell Co., Lynchburg, 3 July; Fluvan-
Maryland, Virginia, and West Virginia, as na Co., SW. of Zion X-Roads, 4 July; Fred-
well as additional counties in western Penn- erick Co., Winchester, 26 June; Montgom-
sylvania (Fig. 2). All collections were made ery Co., Christiansburg, 26 Aug.; Page Co.,
in 1994-1995 by A.G.W. from C. bieber- Luray, 7 Aug.; Prince Edward Co., mt.
steinil. Prospect, 3 July; Pulaski Co., Dublin, 3
MARYLAND: Allegany Co., Oldtown, 2 July; Rappahannock Co., Rt. 211 nr. Thorn-
July; Washington Co., Hagerstown, 26 ton Gap and Page Co. line, 7 Aug.; Rock-
June; Hancock, 2 July. PENNSYLVANIA: bridge Co., Fairfield, 3 July; Rockingham
Clearfield Co., Rt. 879 NE. of Clearfield, Co., Broadway, 25 June; Harrisonburg, 4
12 July; Erie Co., Rt. 832 nr. junc. Rt. 90, July; Shenandoah Co., Mount Jackson, 26
SW. of Erie, 13 July; Jefferson Co., Brook- June; Warren Co., Rt. 55, 3 mi. E. of Stras-
ville, 12 July. VIRGINIA: Alleghany Co., burg, 7 Aug. WEST VIRGINIA: Berkeley
VOLUME 98, NUMBER 1 97
Co., Martinsburg, 26 June; Greenbrier Co., mid-July, and there was no evidence of a
Rt. 311 E. of White Sulphur Springs, 4 second generation.
July; Hampshire Co., Springfield, 2 July; All available information suggests that
Mineral Co., Short Gap, 2 July. U. affinis has only recently become estab-
lished in Pennsylvania. We collected adults
DISCUSSION of this species at several sites that yielded
U. quadrifasciata in Pennsylvania and New
The southward spread of U. quadrifas-
York during 1990-1992 (see Hoebeke
ciata into Maryland, Virginia, and West
1993). Had U. affinis been present in sim-
Virginia might have been predicted given
ilar numbers during the early 1990s, it most
the large numbers encountered during sur-
likely would have been detected at one of
veys in south-central Pennsylvania in the
the sites that falls within its current known
early 1990s (Hoebeke 1993, A.G.W., per-
range in those two states.
sonal observations). Natural dispersal from
Populations of U. affinis found in the Ith-
the north would seem responsible for the
aca, N.Y., area in 1994 may be the result of
more southern populations of this tephritid.
previous releases (1983) in Tompkins
In contrast, populations of U. affinis in
County. Densities much lower than at pres-
eastern North America, at least in Pennsyl-
ent could possibly have gone unnoticed
vania, are more limited in their extent than
during Hoebeke(cid:8217)s (1993) surveys.
those of U. quadrifasciata. Our sampling of
The origin of Pennsylvania populations
spotted knapweed, although based strictly
of U. affinis is even more problematic. No
on sweepnet collecting of adults, was suf-
releases have been documented for the
ficient to detect this fly at 22 other localities
State; Prince George(cid:8217)s Co., Md., and Tomp-
near the site of its initial capture; at most
kins Co., N.Y., are the nearest known re-
sites only 1(cid:8212)5 individuals were observed.
lease sites. Urophora affinis, however, is
Surveys were generally negative for U. af-
not known to be established in Maryland
finis at sites outside an apparent core pop-
(P. W. Tipping, pers. comm. 1994), and we
ulation centered in Schuylkill Co. (Fig. 1),
did not find it in that state in 1994 during
even though the size of knapweed colonies
limited sampling of spotted knapweed in
and sampling intensity were equivalent.
Allegany and Washington counties. If pop-
Negative localities are shown in Fig. 1 only
ulations in eastern Pennsylvania are the re-
if there seemed to be a reasonable chance
sult of natural dispersal from central New
of collecting adults (until about mid-July).
York, the fly could be expected to occur in
We also failed to detect populations in
the intervening area. It was not, however,
northern Pennsylvania and south-central found immediately north and northwest of
New York, as well as in Maryland, Virgin-
Schuylkill Co., Pa.; nor was it detected at
ia, and West Virginia. various other sites in New York and Penn-
Densities of U. affinis adults in Pennsyl-
sylvania (Fig. 1).
vania were not assessed, but field estimates Urophora affinis (and U. quadrifasciata)
indicated that at least during late June to can be purchased from suppliers of biolog-
mid-July they were typically outnumbered ical control agents, but because there is lit-
10(cid:8212)20:1 by U. quadrifasciata. Only at tle interest in controlling spotted knapweed
Pottsville on 7 July 1994 was U. affinis in the East (N. Poritz, pers. comm. 1994),
dominant: about 100 adults vs 4(cid:8212)5 of U. the possibility of this tephritid(cid:8217)s establish-
quadrifasciata; by late July the latter spe- ment from releases by private citizens or
cies was abundant and no U. affinis were local governments seems unlikely. Other al-
found. Tamaqua was the only other site at ternatives are long-distance aerial transport,
which more than 10 U. affinis adults were either active or passive, from established
observed. No U. affinis were seen after populations in New York or Virginia, or
98 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON
through the accidental introduction of in- whether U. affinis becomes the dominant te-
fested knapweeds via commerce. phritid species in most eastern knapweed
Regardless of their origin, the eastern stands.
North American populations of U. affinis
provide an additional opportunity to eval- ACKNOWLEDGMENTS
uate long-term interactions with U. quad- We thank E. R. Hoebeke (Department of
rifasciata. In the West, the latter biocontrol Entomology, Cornell University, Ithaca,
agent initially spread more rapidly, coloniz- NY), A. L. Norrbom (Systematic Entomol-
ing even remote knapweed stands (Harris ogy Laboratory ARS-USDA, Washington,
1980a, Harris and Myers 1984, Story et al. DC), and K. Valley (PDA-BPI) for verify-
1987, Story et al. 1992). But U. affinis ing the identification of U. affinis; R. K.
proved the more persistent of the two spe- Tressler (PDA-BPI) for the figures; J. R.
cies and has generally become dominant at Coulson (USDA, ARS, Beltsville, MD), E.
sites where they co-occur. This is also the R. Hoebeke, L. T. Kok (Department of En-
case in Europe (Berube 1980, Story et al. tomology, VPI & SU, Blacksburg, VA), J.
1992). P. McCaffrey (Department of Plant, Soil
Urophora quadrifasciata disperses more and Entomological Sciences, University of
readily than U. affinis (but does not show Idaho, Moscow), N. Poritz (Biological Con-
greater flight propensity or endurance in trol of Weeds, Bozeman, MT), and P. W.
laboratory studies [Roitberg 1988]) and has Tipping (Plant Protection Section, Mary-
potential for more rapid population in- land Department of Agriculture, Annapolis)
crease. These advantages tend to be offset for providing useful information or sharing
by the lack of unopened inflorescences unpublished data; and E. R. Hoebeke, L. T.
available in late summer. In contrast, the Kok, and K. Valley for reviewing the manu-
univoltine U. affinis emerges when flower script and providing useful suggestions for
buds of its hosts are abundant, and it con- improvement.
sequently has less pressure to disperse. Its
LITERATURE CITED
attacks on knapweed retard further devel-
opment of capitula, placing the mainly bi- Berube, D. E. 1980. Interspecific competition between
voltine, later-emerging U. quadrifasciata at Urophora affinis and U. quadrifasciata (Diptera:
a competitive disadvantage (Berube 1980, Tephritidae) for ovipositional sites on diffuse
knapweed (Centaurea diffusa: Compositae). Zeit-
Harris and Myers 1984, Story et al. 1992).
schrift fiir angewandte Entomologie 90: 299-306.
These seedhead flies by themselves can-
Foote, R. H., EF L. Blanc, and A. L. Norrbom. 1993.
not be expected to reduce host plant den- Handbook of the Fruit Flies (Diptera: Tephritidae)
sities in the East. They have not done so in of America North of Mexico. Cornell University
Press, Ithaca, N.Y. 571 pp.
western North America (Harris and Cran-
Gleason, H. A. and A. Cronquist. 1991. Manual of
ston 1979, Harris 1980a, Maddox 1982,
Vascular Plants of Northeastern United States and
Story et al. 1989), and a (cid:8220)cumulative
Adjacent Canada, 2nd ed. New York Botanical
stress(cid:8217)(cid:8217) approach combining biological con- Garden, Bronx, N.Y. 910 pp.
trol with other management techniques will Harris, P 1980a. Establishment of Urophora affinis
Frfld. and U. quadrifasciata (Meig.) (Diptera: Te-
be needed to achieve successful control
phritidae) in Canada for the biological control of
(Miiller-Scharer and Schroeder 1993). Nev-
diffuse and spotted knapweed. Zeitschrift fiir an-
ertheless, these tephritids should be consid- gewandte Entomologie 89: 504(cid:8212)514.
ered beneficial in the East, their combined . 1980b. Effects of Urophora affinis Frfid. and
attacks on spotted knapweed likely result- U. quadrifasciata (Meig.) (Diptera: Tephritidae)
ing in reduced seed production similar to on Centaurea diffusa Lam. and C. maculosa Lam.
(Compositae). Zeitschrift fiir angewandte Ento-
that documented in the West (Harris 1980a,
mologie 90: 190(cid:8212)201.
1984; Harris and Myers 1984). Their pop- . 1984. Current approaches to biological con-
ulations should be monitored to determine trol of weeds, pp. 95(cid:8212)103. In Kelleher, J. S. and
VOLUME 98, NUMBER 1 99
M. A. Hulme, eds., Biological Control Pro- tomological Society of British Columbia 85: 58(cid:8212)
grammes against Insects and Weeds in Canada 64.
1969-1980. Commonwealth Agricultural Bureaux, Shorthouse, J. D. 1978a. Developmental morphology
Slough, England. of Urophora affinis galls. Proceedings Knapweed
Harris, P and R. Cranston. 1979. An economic eval- Symposium, Oct. 6-7, Kamloops, B.C., pp. 188(cid:8212)
uation of control methods for diffuse and spotted 195.
knapweed in western Canada. Canadian Journal of Shorthouse, J. D. 1978b. Developmental morphology
of Urophora quadrifasciata galls. Proceedings
Plant Science 59: 375-382.
Knapweed Symposium, Oct. 6-7, Kamloops, B.C.,
Harris, P. and J. H. Myers. 1984. Centaurea diffusa
pp. 196-201.
Lam. and C. maculosa Lam. s. lat., diffuse and
Shorthouse, J. D. 1990. Modification of flowerheads
spotted knapweed (Compositae), pp. 127(cid:8212)137. In
of diffuse knapweed by the gall-inducers Uropho-
Kelleher, J. A. and M. A. Hulme, eds., Biological
ra affinis and U. quadrifasciata (Diptera: Tephrit-
Control Programmes against Insects and Weeds in
idae), pp. 221(cid:8212)228. In Delfosse, E. S., ed., Pro-
Canada 1969-1980. Commonwealth Agricultural
ceedings of the VII International Symposium on
Bureaux, Slough, England.
Biological Control of Weeds, Rome, Italy. Istituto
Hoebeke, E. R. 1993. Establishment of Urophora Sperimentale per la Patologia Vegetale (MAF).
quadrifasciata (Diptera: Tephritidae) and Chry-
Story, J. M. and N. L. Anderson. 1978. Release and
solina quadrigemina (Coleoptera: Chrysomelidae) establishment of Urophora affinis (Diptera: Te-
in portions of eastern United States. Entomologi- phritidae) on spotted knapweed in western Mon-
cal News 104: 143-152. tana. Environmental Entomology 7: 445-448.
Julien, M. H., ed. 1992. Biological Control of Weeds: Story, J. M., K. W. Boggs, and W. R. Good. 1992.
A World Catalogue of Agents and their Target Voltinism and phenological synchrony of Uropho-
Weeds, 3rd ed. CAB International, Wallingford, ra affinis and U. quadrifasciata (Diptera: Tephrit-
UK. 186 pp. idae), two seed head flies introduced against spot-
Kartesz, J. T. 1994. A Synonymized Checklist of the ted knapweed in Montana. Environmental Ento-
mology 21: 1052-1059.
Vascular Flora of the United States, Canada, and
Story, J. M., K. W. Boggs, and R. M. Nowierski. 1989.
Greenland, 2nd ed. Vol. 1(cid:8212)Checklist. Timber
Effect of two introduced seed head flies on spotted
Press, Portland, Ore. 622 pp.
knapweed. Montana AgResearch 5(1): 14-17.
Maddox, D. M. 1979. The knapweeds: Their econom-
Story, J. M., R. M. Nowierski, and K. W. Boggs. 1987.
ics and biological control in the western states,
Distribution of Urophora affinis and U. quadri-
U.S.A. Rangelands 1: 139-141.
fasciata, two flies introduced for biological con-
Maddox, D. M. 1982. Biological control of diffuse trol of spotted knapweed (Centaurea maculosa) in
knapweed (Centaurea diffusa) and spotted knap- Montana. Weed Science 35: 145-148.
weed (C. maculosa). Weed Science 30: 76-82. Strang, R. M., K. M. Lindsay, and R. S. Price. 1979.
Miiller, H., D. Schroeder, and A. Gassmann. 1988. Knapweeds: British Columbia(cid:8217)s undesirable ali-
Agapeta zoegana (L.) (Lepidoptera: Cochylidae), ens. Rangelands 1: 141-143.
a suitable prospect for biological control of spot- Turner, C. E., R. Sobhian, D. B. Joley, E.M . Coombs,
ted and diffuse knapweed, Centaurea maculosa and G. L. Piper. 1994. Establishment of Uropho-
Monnet de la Marck and Centaurea diffusa Mon- ra sirunaseva (Hering) (Diptera: Tephritidae) for
net de la Marck (Compositae) in North America. biological control of yellow starthistle in the west-
Canadian Entomologist 120: 109-124. ern United States. Pan-Pacific Entomologist 70:
206-211.
Miiller-Scharer, H. and D. Schroeder. 1993. The bio-
U.S. Department of Agriculture (USDA). 1971. Com-
logical control of Centaurea spp. in North Amer-
mon Weeds of the United States. Dover Publ.,
ica: Do insects solve the problem? Pesticide Sci-
New York. 463 pp.
ence 37: 343-353.
Watson, A. K. and A. J. Renney. 1974. The biology
Myers, J. H. and P. Harris. 1980. Distribution of Uro-
of Canadian weeds. 6- Centaurea diffusa and C.
phora galls in flower heads of diffuse and spotted
maculosa. Canadian Journal of Plant Science 54:
knapweed in British Columbia. Journal of Applied 687-701.
Ecology 17: 359-367.
White, I. M. and V. A. Korneyev. 1989. A revision
Roitberg, B. D. 1988. Comparative flight dynamics of of the western Palaearctic species of Urophora
knapweed gall flies Urophora quadrifasciata and Robineau-Desvoidy (Diptera: Tephritidae). Sys-
U. affinis (Diptera: Tephritidae). Journal of the En- tematic Entomology 14: 327-374.
