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Home , Acraspis, Callirhytis, Cooper (profession), Curculio sayi, Diastrophus, Dryocosmus

BIOLOGY Community Associates of an Exotic Gallmaker, kuriphilus (: Cynipidae), in Eastern North America

1 W. R. COOPER AND L. K. RIESKE

Department of Entomology, University of Kentucky, S-225 Ag North, Lexington, KY 40546-0091

Ann. Entomol. Soc. Am. 100(2): 236Ð244 (2007) ABSTRACT Yasumatsu (Hymenoptera: Cynipidae) is a potentially devas- tating exotic invasive gall that is rapidly spreading throughout the eastern United States, and infests all species of , Castanea spp. We investigated the community associates of D. kuriphilus in three geographic locations: Meadowview, VA, Bowling Green, KY, and Broadview Heights, OH. Dissection of galls and observation of chamber contents revealed that larval mortality is approaching 47%, and parasitism accounts for nearly 70% of the mortality. Six wasp species emerged from chestnut galls, including one introduced species and Þve of unknown origin. The life histories of each parasitoid and their potential roles within the D. kuriphilus community complex are discussed. Investigation of parasitoid interactions revealed a negative correlation between certain , suggesting competition for resources, hyperparasitism, or both. The small chestnut weevil, sayi (Gyllenhal) (Coleoptera: ), caused external damage to galls. Galls also were readily attacked by an unknown fungal pathogen resulting in gall wasp larval mortality. This study is the Þrst to investigate the community associates of D. kuriphilus in North America. Our results have beneÞcial implications for commercial chestnut production, blight resistance breeding programs, and restoration of .

KEY WORDS chestnut, , , Curculio, endophyte

American chestnut, Castanea dentata Marshall (family D. kuriphilus causes signiÞcant damage to chestnut ), was once a codominant canopy species in by forming galls on actively growing shoots that re- forests of the eastern United States (Braun duce tree vigor, prevent normal shoot development 1950, Nelson 1955). In 1904, the exotic and ßowering, and cause branch and tree mortality fungus, Cryphonectria (Endothia) (Murr) (Payne et al. 1975, Kato and Hijii 1997). The gall wasp Barr (Diaporthales: Valsaceae), was accidentally in- is parthenogenetic and univoltine. Adult ovi- troduced and spread quickly throughout the natural posit inside vegetative and mixed buds of Castanea spp. range of American chestnut, functionally eliminating during the summer. Eggs hatch soon after, and larvae the species (Keever 1953, Good 1968, Mackey and remain in the neonate stage until the next growing Sivec 1973, McCormick and Platt 1980). The fungus season. Larval growth begins the next spring, concur- causes diffuse stem cankers that eventually girdle the rent with bud break, when larvae induce the rapid tree, killing the aboveground portions. Today, Amer- formation of conspicuous stem or leaf galls. These galls ican typically exist only as shrubby, non- provide the wasp larvae protection from desiccation fruiting sprouts from surviving stumps, and usually die and predation throughout the remaining larval stages back after reaching 2Ð3 m in height (Paillet 1984, and through pupation. Adults are active for Ϸ1mo 2002). Tree breeders and geneticists have worked after emergence from galls and move to newly formed diligently to breed blight resistance from Asian chest- buds for oviposition. After adult emergence, galls desic- nuts (Castanea spp.) into American chestnut, and cate and become woody, and they can remain on the trees for restoration could be available within the next tree for several years. several years (Anagnostakis 2001). However, another A native of , D. kuriphilus was a major in more recent exotic pest, Dryocosmus kuriphilus Ya- Japan and Korea after accidental introductions (Ya- sumatsu (Hymenoptera: Cynipidae), is now threaten- sumatsu 1951, Murakami et al. 1995). Asian chestnut ing American chestnut in the eastern United States varieties resistant to galling were initially used for and could impact restoration programs (Anagnostakis management. However, virulent gall wasp isolates 2001, Schlarbaum et al. 2001). soon became dominant, eliminating the efÞcacy of host plant resistance as a management tool (Shimura 1972). In the 1970s, the parasitic Torymus sinensis 1 Corresponding author, e-mail: [email protected]. Kamijo (Hymenoptera: ) was collected

0013-8746/07/0236Ð0244$04.00/0 ᭧ 2007 Entomological Society of America March 2007 COOPER AND RIESKE:CHESTNUT GALL WASP COMMUNITY ASSOCIATES 237 from China and released in Japanese orchards (Mu- rakami et al. 1977, 1980). As a result of T. sinensis parasitism, D. kuriphilus populations rapidly declined below tolerable levels (Moriya et al. 1989, 2003). D. kuriphilus was Þrst observed in the United States infesting Chinese chestnut, C. mollissima Blume, near Byron, GA (Peach Co.), in 1974. It is thought to have been accidentally introduced on chestnut nursery stock from Asia (Payne et al. 1975). In the decade after its introduction, the gall wasp nearly eliminated the chestnut in Georgia (Anagnostakis and Payne 1993). In addition to commercially planted chestnuts, ornamental Chinese chestnuts also serve as suitable hosts and are planted throughout the United States. D. kuriphilus also threatens efforts to restore American chestnut as a viable component of the Appalachian forest (Anagnostakis 1999, Schlarbaum et al. 2001). In 1977, several parasitoids, including Torymus spp., were introduced to Georgia from Japan with hopes of pro- viding biological control against D. kuriphilus (Payne 1978). However, the establishment and efÞcacy of these releases and the dispersal of the parasitoids were not tracked. Consequently, we do not fully understand the ability of these parasitoids to establish themselves and disperse with expanding gall wasp populations, nor do we fully understand the role parasitoids may play in regulating chestnut gall wasp populations in Fig. 1. Initial introduction of D. kuriphilus near Bryon, GA, in 1976. Galls for current study were collected near the eastern United States. Many cynipid wasps, in- Meadowview, VA, Bowling Green, KY, and Broadview cluding other Dryocosmus species, form galls on Heights, OH. Historic range of American chestnut in eastern (Quercus spp.) in eastern North America, and many North America is in shaded gray (USGS 1999). parasitoids associated with these gall makers could potentially use D. kuriphilus as a host (Payne 1978). Despite its 30ϩ years in the United States, very little throughout the farm (Cooper and Rieske-Kinney is known about the ecological relationships, dispersal, 2006). or population regulation of D. kuriphilus in North The Bowling Green, KY, collection site (Warren America, and much of the information known is an- Co.) (36Њ 57Ј N, 86Њ 33Ј W) is located on the boundary ecdotal (Aebi et al. 2006). The goal of our work is to of the Pennyroyal and Shawnee Hills physiographic characterize the associates of D. kuriphilus in eastern regions and is near the western edge of the original North America, speciÞcally focusing on introduced range of American chestnut (Braun 1950, McEwan et and native natural enemies, to determine what factors al. 2005) (Fig. 1). It is also the western-most recorded regulate gall wasp populations. Our ultimate goal is to occurrence of D. kuriphilus. This site is located in a gain a more complete understanding of the ecological privately owned forest where several tall (5Ð15 m) interactions, dispersal patterns, and mechanisms reg- naturally occurring American chestnut trees persist, ulating D. kuriphilus populations in eastern North despite infection with the blight fungus. The chestnut America. gall wasp occurs on a single tree at this site and was Þrst observed in winter 2003Ð2004 (Cooper and Rieske- Kinney 2006). Materials and Methods The third collection site is in a suburban setting in Collection Sites. Galled plant material was collected Broadview Heights, OH (Cuyahoga Co.) (41Њ 20Ј N, from three geographically distinct locations (Fig. 1). 81Њ 39Ј W) located in the Erie Lake Plain physi- The Þrst, in Meadowview, VA (Washington Co.) (36Њ ographic region near the northwest border of the 45Ј N, 81Њ 51Ј W), is located at the American Chestnut original range of American chestnut (Braun 1950) FoundationÕs breeding farm. Meadowview is located (Fig. 1). The location is made up mostly of suburban in the Ridge and Valley physiographic region and is housing, and chestnut in the immediate area is limited within the original range of American chestnut (Braun to three mature ornamental Chinese chestnuts located 1950) (Fig. 1). Trees growing on the site are used for on two adjacent privately owned properties in Broad- the FoundationÕs blight resistance breeding efforts, view Heights. The infestation was Þrst recorded in and they are arranged in evenly spaced and age-syn- 2003 (Stehli 2003). chronized blocks of American, Chinese, or In addition to the collection sites described above, chestnuts. The area is surrounded by farms, pasture- on 30 April, 31 naturally occurring American chestnut land, and hardwood woodlots. The initial gall wasp saplings along ridge tops in the Red River Gorge Geo- infestation was noticed in 2001 and rapidly spread logical Area, in the Cliff Section of the Cumberland 238 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 100, no. 2

Fig. 2. D. kuriphilus mandibles (A) are large and ßat, whereas parasitoid mandibles (B) are comparatively small and sharp.

Plateau in eastern Kentucky (Wolfe Co.) (37Њ 47Ј N, tion (Department of Entomology, University of Wis- 83Њ 40Ј W), were visually examined for galling caused consin, Madison, WI). The incidence of parasitoid by D. kuriphilus. emergence was recorded as the number of wasps per Gall Collection. Chestnut shoots containing current gall per tree; emergence values represent the rates of and previous generation galls were collected from emerging parasitoid adults, and they may not repre- each site at 3-wk intervals from before bud break to sent the actual rates of parasitism. after D. kuriphilus adult emergence. In Meadowview, Gall Associates and Parasitism Rates. In addition to VA, two shoots per tree (one each from the east and the sequential collections, 341 current generation galls west aspect), each containing Ϸ20Ð30 galls per tree, also were collected from 20 American chestnut trees were collected from Þve American and Þve Chinese in Meadowview on 15 June, just before D. kuriphilus chestnut trees from 30 March to 22 June. In Bowling pupation. The exterior of each gall was carefully ex- Green, KY, three shoots, each containing Ϸ20Ð30 amined for signs of herbivory or pathogen infection. galls, were collected from American chestnut from 7 Each gall was then dissected under an 8.82ϫ dissecting April to 2 July. Because the Bowling Green site was scope to determine the number of chambers per gall made up of a single tree, collections were replicated and the contents of each chamber. D. kuriphilus larvae only by shoot. In Broadview Heights, three shoots per and parasitoids were identiÞed by examining the man- tree, each with Ϸ20Ð30 galls, were collected from dibles. D. kuriphilus larvae have large ßat mandibles Chinese chestnut 22 April to 7 July. Shoots were specialized for grazing on the inner tissues of the galls clipped at the second apical growth scar to ensure only (Fig. 2A). In contrast, parasitoids such as T. sinensis 2 yr of growth. Clipped shoots were bagged and kept have comparatively small sharp mandibles (Fig. 2B) cool during transport to the laboratory. for feeding on the gall former, allowing the parasitoid To separate the current generation from the pre- to subsequently use the gall chamber for its own de- vious generationÕs galls, all shoots were cut at the velopment (Njentes-Aldry et al. 2005). previous yearÕs apical growth scar in the laboratory. Statistical Analyses. To determine whether parasi- Current generation galls (n ϭ 10Ð15 per tree) are toids show a preference between American and Chi- green, pliable, living galls that developed during the nese chestnuts, the incidence of emergence of the two study in spring 2005 and contain within them D. ku- most abundant parasitoids were compared between riphilus, parasitoids of D. kuriphilus, or both. Previous the two chestnut species in Meadowview, by using a generation galls (n ϭ 10Ð15 per tree) are dark brown, standard t-test. Occurrences of the remaining parasi- desiccated woody galls that developed in spring 2004 toids were not great enough to compare statistically. and do not contain D. kuriphilus , but they may Parasitoid emergence between collection sites was contain parasitoids or associates of D. kuriphilus. compared using TukeyÕs honestly signiÞcant differ- Galled plant material (current and previous) was ence (HSD) and paired t-tests derived from contrast placed in 500-ml containers with moist sand and statements. To investigate potential interactions be- placed under separate cylindrical cages (30.5 by 61 tween T. sinensis and pooled native parasitoids (n ϭ 5 cm) darkened with Þne mesh screen, with a transpar- species), we used a multivariate canonical correlation ent inverted cone Þtted with an 8-ml collection vial analysis (PROC CANCORR, SAS Institute 1999) and (Choate and Rieske 2005). Cages were monitored the standardized canonical coefÞcients to assess rela- daily during each 3-wk interval for gall wasp or para- tionships among variables. All data were normalized sitoid emergence. Galled shoot material was ex- using a log transformation. Mean abundance, richness, changed with fresh collections from each site at the Simpson diversity index, and Pielou evenness index end of each 3-wk interval. Wasps and associates were were calculated (PC-ORD, McCune and Mefford stored in 70% ethanol and identiÞed. Voucher speci- 1999) and compared between collection sites using mens were deposited at the Research Collec- TukeyÕs HSD. March 2007 COOPER AND RIESKE:CHESTNUT GALL WASP COMMUNITY ASSOCIATES 239

Table 1. D. kuriphilus emergence (mean ؎ SE) from galls chestnut trees (Anagnostakis 1999). We suspect that collected from three sites in eastern North America the Broadview Heights gall wasp infestation resulted from movement of infested nursery stock or other No. of D. kuriphilus No. of galls Collection site D. kuriphilus infested material, although the possibility of a second adults/gall examined emerging U.S. introduction cannot be discounted. Meadowview, VA 0.08 Ϯ 0.04b 4 63 To determine the extent of parasitism of D. kuriphi- Bowling Green, KY 1.1 Ϯ 0.2a 14 13 lus larvae, galls (n ϭ 341) were dissected before adult Broadview Heights, OH 0.17 Ϯ 0.03b 5 55 D. kuriphilus emergence. Chamber contents fell into F ϭ 42.16, df ϭ 2, P Ͻ 0.0001 three categories: living D. kuriphilus larvae (53.2%), living parasitoid larvae (32.6%), or empty chamber (14.3%). Because each gall chamber was formed by a Results and Discussion D. kuriphilus larva, the rate of larval mortality in the Adult D. kuriphilus was collected at each site and galls is the number of chambers with living parasitoids emerged between 7 and 10 July in Meadowview, 21Ð27 plus the empty chambers and was 46.8%. Parasitism June in Bowling Green, and 12Ð17 July in Broadview (chambers with living parasitoid larvae/total D. ku- Heights, corresponding to Ϸ770Ð780ЊC degree-days riphilus mortality) accounted for 69.5% of the mor- (DD , start date, 1 January) at each location tality, although parasitoid larvae could not be identi- base 10ЊC (Johnson et al. 1998). Emergence was signiÞcantly Þed to taxa. greater in Bowling Green and was not different between Six parasitoid species were collected as adults Meadowview and Broadview Heights (Table 1). emerging from D. kuriphilus galls, including the in- Natural dispersal of D. kuriphilus by ßight in the troduced Torymus sinensis (Fig. 3A), Ormyrus labotus eastern United States occurs at a rate of 24 km/yr Walker (Hymenoptera: ) (Fig. 3B), and (Payne 1981). Nearly 25 yr after its initial introduction four less abundant species of unknown origin. Our in Georgia, D. kuriphilus was reported in chestnut data suggests that T. sinensis and O. labotus may be orchards throughout Georgia, and into Alabama, abundant enough to affect gall wasp populations (Ta- North Carolina, and Tennessee (Anagnostakis et al. bles 2 and 3), but the remaining four genera were 1993; Anagnostakis 1999, 2001). The gall wasp infes- collected in very low frequencies (Table 3). Only T. tation in Meadowview (2001) and Bowling Green sinensis was previously known to parasitize D. kuriphi- (2003) most likely occurred through natural move- lus, although other species in the genera Ormyrus, ment of dispersing wasps and is consistent with the Sycophila, and Pteromalus also parasitize D. projected rate of ßight dispersal. However, as summer kuriphilus. 2006, D. kuriphilus has not been recorded from any The most abundant parasitoid, T. sinensis, was ab- other location in Kentucky, and naturally occurring sent from Bowling Green and was reared only from chestnut saplings sampled in the Red River Gorge area previous generation galls collected at Meadowview of eastern Kentucky showed no signs of infestation in and Broadview Heights (Table 2). The incidence of T. April and May 2005. In contrast, Broadview Heights is sinensis (n ϭ 36) differed marginally among collection nearly twice the distance from the initial Byron, GA, sites (t ϭ 3.43, df ϭ 1, P ϭ 0.06), with the greatest introduction. This distance exceeds the projected rate abundance in Broadview Heights (Table 2). T. sinensis of dispersal by ßight and most likely represents a (n ϭ 26) emerged from both American and Chinese satellite infestation. Before 2001, D. kuriphilus was chestnut galls collected from Meadowview between 5 reported in McMinnville, TN, an area with extensive April and 12 April, and it did not differ signiÞcantly nursery production and a hub for mail order sales of between American and Chinese chestnuts (t ϭ 0.22,

Fig. 3. The two most abundant parasitoids, T. sinensis (A) and O. labotus (B) emerging from D. kuriphilus galls collected near Meadowview, VA, Bowling Green, KY, and Broadview Heights, OH. 240 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 100, no. 2

Table 2. The two most abundant parasitoid species emerging control agent in Japan, and the high emergence rate .mean ؎ SE parasitoids per gall per tree) from current and previous observed in Meadowview and Broadview Heights, T) year’s D. kuriphilus galls collected from American and Chinese chestnut at three sites sinensis seems to be playing a major role in population regulation of D. kuriphilus in the United States. Parasitoid adults emerged (no. of galls examined) The distribution of T. sinensis in our collections Meadowview, Bowling Broadview (present in Meadowview and Broadview Heights, ab- VA Green, KY Heights, OH sent in Bowling Green) (Table 2) provides insight into T. sinensis the dispersal patterns and ecological relationships be- Previousa 0.55 Ϯ 0.14ab (68) 0b (14) 0.71 Ϯ 0.19a (58) tween the gall wasp and its introduced parasitoid. The O. labotus Currentb 0.12 Ϯ 0.05b (58) 0.41 Ϯ 0.05a (13) 0.02 Ϯ 0.02b (58) D. kuriphilus infestation in Bowling Green is relatively Previousa 0.14 Ϯ 0.1a (68) 0a (13) 0.02 Ϯ 0.02a (55) recent, and establishment of an introduced parasitoid Total 0.28 Ϯ 0.13a (126) 0.19 Ϯ 0.05a (26) 0.02 Ϯ 0.04a (113) by ßight dispersal would undoubtedly lag behind that of the host insect. Apparently the dispersal of the Means within rows with different letters are signiÞcantly different introduced parasitoid has not caught up with the nat- at ␣ ϭ 0.05 (TukeyÕs HSD). a Previous year D. kuriphilus galls. ural dispersal of its gall wasp host in the Bowling Green b Current year D. kuriphilus galls. area. In addition, the Bowling Green collection site is relatively inconspicuous and is limited to a single tree within a heterogeneous woodlot, which undoubtedly df ϭ 1, P ϭ 0.65). T. sinensis emerged from Chinese would affect the success of host Þnding by T. sinensis. chestnut galls collected from Broadview Heights on 21 An additional explanation for the absence of T. sinensis April (Table 2). in Bowling Green could be that competition and/or T. sinensis is a common parasitoid of D. kuriphilus in hyperparasitism may negatively impact its establish- its native range of China, and it was purposefully ment at this location (see below). introduced to Japan in 1980 to help control D. ku- Emergence of T. sinensis from galls collected from riphilus populations (Murakami et al. 1977, Otake et al. the apparent satellite gall wasp infestation in Broad- 1984). Before the introduction of T. sinensis, the gall view Heights suggests that the parasitoid was moved wasp had been the most signiÞcant pest of chestnut in with D. kuriphilus on infested plant material. D. ku- Japan (Moriya et al. 1989). Within several years after riphilus can be difÞcult to detect throughout most of its introduction, parasitism by T. sinensis signiÞcantly the year because larvae are contained within normal- reduced gall wasp outbreaks and provided sustainable looking buds from midsummer until the next spring. T. control throughout Japan (Moriya et al. 1989, 2003). sinensis, however, is only contained within visible cur- Like D. kuriphilus, T. sinensis is univoltine. However, rent generation galls or withered overwintering galls. in contrast to its host, T. sinensis adults emerge in the Although Þnding T. sinensis at the Broadview Heights early spring and oviposit inside developing galls. Lar- site is encouraging from the perspective of a potential vae consume the gall former and remain in the galls population regulator of D. kuriphilus, it strongly im- until the next spring. plies that plant material was transported with obvious Several strains of T. sinensis have been identiÞed galling present, and highlights the need for precau- based on differences in adult emergence. Strains na- tions in transporting invasive (Chornesky et al. tive to Korea and Japan emerge too early to provide 2005). effective control of D. kuriphilus, and instead they The second most abundant parasitoid, O. labotus, exploit galling cynipids as hosts (Murakami et al. was reared from all three sites, and it was present in 1995). The T. sinensis strain native to China and re- both current and previous generation galls (Table 2). leased in Japan is phenologically synchronized with Emergence of O. labotus from current generation galls the life cycle of D. kuriphilus, enhancing its effective- differed between collection sites (F ϭ 7.64, df ϭ 1, P ϭ ness as a population regulator (Moriya et al. 2003). 0.006) and was greatest in Bowling Green (Table 2). Several Asian Torymus species were released in south- Total emergence, and emergence from previous gen- eastern Georgia for control of D. kuriphilus (Payne eration galls, did not differ between collection sites 1978), but this is the Þrst published account of its (F ϭ 0.87, df ϭ 2, P ϭ 0.44 and F ϭ 0.51, df ϭ 2, P ϭ successful establishment in the United States. Given 0.61, respectively) (Table 2). O. labotus (n ϭ 7) the success of T. sinensis as a sustainable biological emerged from previous generation chestnut galls col- lected in Meadowview from 4 to 8 April, but its oc- currence did not differ between chestnut species (t ϭ Table 3. Minor parasitoid emergence (mean no. per gall per ϭ ϭ ϭ tree) from D. kuriphilus galls from American and Chinese chestnut 0.31, df 1, P 0.59). Parasitoid emergence (n 7) trees from three sites from current yearÕs American and Chinese chestnut galls occurred on 16 May and on 15 July. O. labotus Parasitoid Meadowview, Bowling Broadview (n ϭ 5) only emerged from current generation galls in species VA Green, KY Heights, OH Bowling Green between 23 and 27 June. In Broadview S. mellea Ͻ0.01 (1) 0 0 Heights, emergence from previous seasonÕs galls oc- P. minio 00Ͻ0.01 (1) curred on 23 April (n ϭ 1) and from current seasonÕs E. sp. 0 Ͻ0.01 (2) 0 ϭ Pteromalus sp. Ͻ0.01 (1) 0 0 galls on 13 June (n 1). The difference in O. labotus emergence among our sites may be due to habitat Values in parentheses indicate the total number emerged. variability. O. labotus is a major parasitoid of oak- March 2007 COOPER AND RIESKE:CHESTNUT GALL WASP COMMUNITY ASSOCIATES 241 galling insects, and Quercus spp. is a major component specimen may have emerged from a host other than D. of woodlots surrounding Meadowview and Bowling kuriphilus. Green. In contrast, Broadview Heights is a suburban Eupelmus sp. was represented by a single specimen area that may lack signiÞcant oak dominated woodlots that could not be identiÞed to species. It emerged from as a potential source of O. labotus. O. labotus is among a current generation gall collected in Bowling Green the most abundant parasitoids of the horned oak gall, on 6 July (Table 3). The genus has a cosmopolitan Callirhytis cornigera Osten Sacken (Hymenoptera: distribution (Burks 1979, Noyes 2003) and several Cynipidae), in central Kentucky (Eliason and Potter species parasitize D. kuriphilus, or hyperparasitize T. 2000). It is a generalist parasitoid of gall formers and sinensis in other regions infested with D. kuriphilus has been recorded emerging from galls in the cynipid (Otake et al. 1982, Murakami et al. 1994, 1995; Aebi et genera Acraspis, Callirhytis, Ceroptres, Diastrophus, al. 2006). Eupelmus spp. commonly parasitize oak gall Disholcaspis, and (Burks 1979, Washburn formers in North America (Askew 1961, Noyes 2003), and Cornell 1979, Eliason and Potter 2000, Noyes and it is likely associated with oak-galling insects. 2003). This is the Þrst report of O. labotus parasitizing Finally, Pteromalus sp. also was represented by a Dryocosmus. However, congeneric species have been single specimen that could not be identiÞed to species. recorded parasitizing D. kuriphilus in other regions It emerged from a current generation gall collected in (Murakami et al. 1980, Otake et al. 1982, Kim 1998, Meadowview on 6 July (Table 3). Pteromalus spp. also Aebi et al. 2006). has a cosmopolitan distribution, and members of this In addition to the two parasitoid species collected in genus are parasitoids and hyperparasitoids of a large abundance, we collected several other species in number of insect hosts, including Eupelmus spp. lower frequencies, including Sycophila mellea Walker (Noyes 2003). Only one species in Japan, Pteromalus (Hymenoptera: ), Pnigalio minio Walker apantelophagus Crawford, is recorded parasitizing D. (Hymenoptera: ), Eupelmus sp. (Hyme- kuriphilus (Otake et al. 1982). It is not known whether noptera: ), and Pteromalus sp. (Hymenop- this Pteromalus sp. is a parasitoid associated with D. tera: ). S. mellea is represented by two kuriphilus or a hyperparasitoid in North America. specimens collected in Meadowview on 25 and 27 The abundance of D. kuriphilus community associ- June from current generation American chestnut galls ates was signiÞcantly greater in Broadview Heights (Table 3). It is a generalist parasitoid of cecidomyiid (F ϭ 4.97, df ϭ 2, P ϭ 0.03), most likely due to the ßies (Diptera: ), certain aphids (Hemip- relative abundance of T. sinensis. Rapid parasitoid re- tera: Aphididae), and eurytomid wasps (Hymenop- cruitment by D. kuriphilus has been demonstrated in tera: Eurytomidae) (Burks 1979, Dubbert et al. 1998, other regions of its range expansion (Aebi et al. 2006); Noyes 2003). Several Sycophila spp. also are associated however, we found no differences in diversity, rich- with gall-forming cynipids on oaks in North America ness, or evenness of D. kuriphilus associates, in spite of (Eckberg and Cranshaw 1994, Zuparko 1996, Eliason habitat differences and differences in D. kuriphilus and Potter 2001). Other species within this genus, residence time between our collection sites. including Sycophila variegata Curtis, Sycophila con- The trends we observed in parasitoid emergence cinna Boheman, and Sycophila biguttata Swederus, provide insight into potential interactions between which have been recorded emerging from D. kuriphi- the parasitoids and the gall wasp, and between para- lus galls in China, Korea, Japan, and (Yasumatsu sitoid species. The highest incidence of gall wasp and Kamijo 1979; Murakami et al. 1980, 1994, 1995; Luo emergence occurred in Bowling Green, which also and Huang 1993; Aebi et al. 2006). Given the biology had the highest occurrence of the native O. labotus, of this genus in other regions infested with D. kuriphi- and where the introduced T. sinensis did not occur. lus, it is likely that S. mellea is associated with oak- Gall wasp occurrence was lower in the satellite Broad- galling wasps near the Meadowview collection site view Heights infestation, where the emergence of T. and is also capable of using D. kuriphilus as a host. sinensis was greatest, and the emergence of oak galling P. minio was represented by a single male specimen parasitoids was lowest. Our canonical correlation anal- collected from a current generation gall on 12 June in ysis shows a marginally signiÞcant negative correlation Broadview Heights (Table 3). It also is a generalist between parasitoids of oak-galling insects (O. labotus, parasitoid that uses hosts from 16 insect families in four S. mellea, P. minio, Eupelmus spp., and Pteromalus spp.) orders (Burks 1979, Heyerdahl and Dutcher 1985, and the introduced D. kuriphilus parasitoid, T. sinensis Nystrom and Evans 1989, Duncan and Pena 2000, (F ϭ 2.26; df ϭ 4, 26; P ϭ 0.09). Although our sample Petrice et al. 2000, Gates et al. 2002, Noyes 2003). P. sizes were small, these results support our observa- minio has not been recorded parasitizing cynipid tions and suggest a negative correlation between the wasps, but it is most commonly associated with leaf- introduced T. sinensis and native parasitoids associated mining lepidopterans. However, P. nemati Westwood with oak-galling insects. The habitat differences is a primary parasitoid of the gall-forming sawßy Pon- among our collection sites, parasitoid interactions tania proxima Lepeletier (Hymenoptera: Tenthredi- caused by adult competition for oviposition sites, lar- nidae) on crack , Salix fragilis L. (Salicaceae) val competition for suitable hosts, or hyperparasitism, (Al-Saffar and Aldrich 1998). P. minio may be associ- may play a role in driving this trend. Whether this ated with D. kuriphilus galls in Bowling Green; how- trend is widespread on naturally occurring American ever, we cannot fully discount the possibility that this chestnut saplings in areas of the eastern U.S. where D. 242 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 100, no. 2 kuriphilus is established is unknown and warrants fur- phytes also may have antixenotic effects on gall wasps; ther investigation. for example, gall-forming insects avoid endophyte in- Our results have implications for managing expand- fected tissue during oviposition (Wilson and Carroll ing D. kuriphilus populations. Currently, there is no 1997). The fungus observed on D. kuriphilus galls may effective chemical control for D. kuriphilus because it be a naturally occurring foliar endophyte that war- is protected within the gall throughout most of its life rants further investigation. cycle. Cultural control recommendations involve Our data provide insight into the dispersal patterns pruning and burning visible galls (Payne et al. 1976, of D. kuriphilus in North America, the natural enemies Ahn et al. 1984). D. kuriphilus is present in galls only potentially regulating these D. kuriphilus populations, during the spring in which they develop, after which and potential interactions between parasitoids asso- the galls only house parasitoids that could help regu- ciated with chestnut galls. This is the Þrst report of an late the next D. kuriphilus generation. Our data dem- association between C. sayi and D. kuriphilus, and the onstrate that the most numerous parasitoids emerged Þrst report of a potentially pathogenic fungus that from previous generation galls. Consequently, prun- causes death of D. kuriphilus. Our work expands our ing these galls could have a negative impact on natural knowledge base of D. kuriphilus and its associated enemies of the gall wasp, and a positive impact on D. community in eastern North America, and is essential kuriphilus. Leaving previous generation galls on the for minimizing the negative effects of expanding gall tree would allow parasitoids to complete development wasp populations. and promote gall wasp parasitism and could contribute to sustainable control of D. kuriphilus. In addition to the parasitoids collected, we observed Acknowledgments gall herbivory by the small chestnut weevil, Curculio sayi (Gyllenhal) (Coleoptera: Curculionidae), which We thank Fred Hebert, Ed Stehli, and Steve Hartman for feeds on chestnut seed as larvae and adults (Drooz gall wasp collections. We also thank Steven Krauth (Insect 1985). Females oviposit inside chestnuts, and larvae Research Collection, University of Wisconsin) for identiÞ- feed on the endoderm. We found signs of adult feeding cation of collected wasps and weevils. Tom Coleman, Aerin consisting of small puncture wounds that extended Land, Preeyanhut Phumkhem, and Kevin Pitz provided tech- nical assistance. This research was funded by the American deep into the ßeshy outer layers of the gall, and which Chestnut Foundation, the Northern Nut Growers Associa- were accompanied by a brown oxidation streak ex- tion, and McIntire Stennis funds from the Kentucky Agri- tending from the exterior wound site. Weevil feeding cultural Experimental Station and is published as Experiment was evident on 16% of the collected galls. Cynipid galls Station Project 06-08-108. are chemically similar to seeds (Schonrogge et al. 2000), and these similarities may allow adult weevils to use, or perhaps mistake, cynipid galls for a food and References Cited oviposition resource. Although we observed adult feeding on the galls, we did not observe egg deposition Aebi, A., K. Schonrogge, G. Melika, A. 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