South Dakota State University Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange

Oak Lake Field Station Research Publications Oak Lake Field Station

10-20-2013 The wS itchgrass Gall Midge (Chilophaga virgati Gagné) in the Northern Great Plains Veronica Calles Torrez

Follow this and additional works at: https://openprairie.sdstate.edu/oak-lake_research-pubs

Recommended Citation Torrez, Veronica Calles, "The wS itchgrass Gall Midge (Chilophaga virgati Gagné) in the Northern Great Plains" (2013). Oak Lake Field Station Research Publications. 28. https://openprairie.sdstate.edu/oak-lake_research-pubs/28

This Article is brought to you for free and open access by the Oak Lake Field Station at Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange. It has been accepted for inclusion in Oak Lake Field Station Research Publications by an authorized administrator of Open PRAIRIE: Open Public Research Access Institutional Repository and Information Exchange. For more information, please contact [email protected]. Bioenerg. Res. (2014) 7:417–423 DOI 10.1007/s12155-013-9386-4

The Switchgrass Gall Midge (Chilophaga virgati Gagné) in the Northern Great Plains

Veronica Calles Torrez & Paul J. Johnson & Arvid Boe

Published online: 20 October 2013 # Springer Science+Business Media New York 2013

Abstract Switchgrass (Panicum virgatum L.) is considered to Keywords Chilophaga virgati . . Panicum be a highly promising bioenergy crop. However, little is known virgatum . Platygasterchilophagae . Quadrastichus . about pests that impact its utilization for this purpose. Parasitoid . Phenology . Life history The switchgrass gall midge [Chilophaga virgati Gagné (Diptera: Cecidomyiidae)], which was first discovered in 2008 at Brookings, SD, USA, is shown to have a negative Introduction impact on biomass and seed yields of switchgrass. Our objec- tives were to increase knowledge of the biology of the midge Switchgrass (Panicum virgatum L.) is highly regarded for by describing its life stages and any parasitoids that have feedstock production as a bioenergy crop in North America biological control potential. Data collections were made during and Europe [1]. It was selected because of its high-net energy MaytoDecemberin2011andApriltolateautumnin2012. yield per acre, lower cost of production compared to annual The gall midge adult is active from early June to late July. This crops, low nutrient requirements, high-water use efficiency insect overwinters as a late instar larva, usually in large aggre- [2], environmental benefits [3], and wildlife habitat [4]. So far, gations, enclosed in the sheath of the flag leaf of dry tillers. The only a few pests are associated with switchgrass [5–9]. The mean number of larvae was 31, with a range of 6 to 85 per switchgrass moth, Blastobasis repartella (Dietz), is the most tiller. Infested tillers m−2 varied among three phenologically investigated insect pest on switchgrass, causing tiller death distinct cultivars. The late flowering cultivar ‘Cave-In-Rock’ during late spring in South Dakota [7, 9] and other regions of was more heavily infested (>2×) than the early flowering the Great Plains and Upper Midwest [10]. ‘Dacotah’. A newly discovered parasitoid, Platygaster The switchgrass gall midge, Chilophaga virgati Gagné chilophagae Buhl (Hymenoptera: Platygastridae) and a species (Diptera: Cecidomyiidae), was first discovered in 2008 in a of Quadrastichus sp. (Hymenoptera: Eulophidae) were reared breeding nursery of switchgrass at Brookings, SD, USA. When from gall midge larvae. These results will be valuable to ento- first discovered, the insect had a direct negative impact on mologists, switchgrass breeders, and agronomists as a guide to biomass and seed yield [11] by its feeding at the apical inter- the occurrence and activities of the gall midge. node and peduncle base. It infested up to 22 % of reproductive tillers in a 10-genotype polycross with natural population ori- V. Calles Torrez gins from Illinois, Kansas, and Nebraska. Differences were Department of Entomology, North Dakota State University, Fargo, ND 58108-6050, USA found among the 10 genotypes for percent of tillers infested e-mail: [email protected] [11], suggesting the potential of genetic variation for tolerance to the gall midge. This gall midge has also been observed on * P. J. Johnson ( ) ornamental and agronomic switchgrass plants in South Dakota, Insect Biodiversity Lab, Department of Plant Science, South Dakota State University, Box 2207A, Brookings, SD 57007, USA Minnesota, Nebraska, Illinois, Oklahoma, New York, and New e-mail: [email protected] Jersey, but its complete geographical range is not known nor its relative impact on production in these areas. A. Boe The genus Chilophaga Gagné contains eight species, five Department of Plant Science, South Dakota State University, Box 2140C, Brookings, SD 57007, USA of which are from North America [11, 12]. The species occur e-mail: [email protected] from Canada to Argentina [13]. The genus belongs to the tribe 418 Bioenerg. Res. (2014) 7:417–423

Alycaulini, which contains nine genera and 225 described Agropyron repens (L.) in Pennsylvania [12]. On the other species [12]. Most species of this tribe are found in stem hand, larvae of switchgrass gall midge cause 100 % seed loss swellings, but some live in leaf petioles, vein swellings, blister in infested tillers [11]. In addition, infested tillers are shorter galls of leaves, and a few in flowers [12]. and lighter due to reduction of internode elongation and Larvae of numerous species of Cecidomyiidae prevent seed development at the base of the inflorescence. formation in grasses and cause economic impact [14]. Gagné Damage caused by gall midges on grasses may be lessened [12] reported gall midges feeding on species from 29 genera of by parasitoids. A recently discovered species Platygaster Poaceae in North America. The most common species of gall chilophagae Buhl (Hymenoptera: Platygastridae) is a parasit- midge on non-food crop forage and biomass grasses in North oid of the switchgrass gall midge larvae [22]. The wasp America are in the genera Stenodiplosis Reuter and Aprostocetus nebraskensis (Girault) (Hymenoptera: Calamomyia Gagné [12]. An introduced species to the Great Eulophidae) is a parasitoid of Stenodiplosis wattsi larvae [17], Plains, the bromegrass seed midge [Stenodiplosis bromicola while another eulophid (Tetrastichus sp.) parasitized >90 % of (Marikovski and Agafonova)], caused >50 % seed loss in pupae of the bromegrass midge in Nebraska [15]. Reported smooth bromegrass (Bromus inermis Leyss) in Nebraska parasitoids on other species of Cecidomyiidae are mostly from [15, 16]. Upwards of 40 % of seed production of ‘Pawnee’ big the families Platygastridae, Pteromalidae, and Torymidae and bluestem (Andropogon gerardii Vitman) was destroyed by the less commonly are species from Ceraphronidae, Encyrtidae, bluestem seed midge (Stenodiplosis wattsi Gagné) in Nebraska Eupelmidae, Eulophidae, Braconidae, and Ichneumonidae [17]. This species is widespread in the Great Plains [16, 18]and [12, 15, 23, 24]. has also caused 20 % reduction in seed yields of little bluestem The phenology of switchgrass varies widely among culti- [Szhizachyrium scoparium (Micheaux)] [17]. The gall midge, vars based on latitude of origin. ‘Dacotah’ which is from Calamomyia inustorum (Felt), causes discoloration in stems of North Dakota is shorter and earlier flowering compared with switchgrass in South Dakota and Oklahoma [12],butitisnot ‘Sunburst’ and ‘Cave-In-Rock’ [25]. ‘Dacotah’ flowered in economically significant. Other potential biofuel grasses, such as early July and reached mature seed in August [25, 26], where- Spartina alterniflora Loisel, serve as gall midge hosts, including as ‘Sunburst’, from South Dakota, flowered during early a Stenodiplosis sp. in North Carolina, and Calamomyia August [25] and Cave-In-Rock, from Illinois, flowered during alterniflorae Gagné in Maine and North Carolina. Another late August in the Northern Great Plains [25, 26]. Calamomyia sp. was found in Spartina cynosuroides (L.) in Boe and Gagné [11] provided preliminary information North Carolina [12]. The ecological and agronomic impact of regarding potential impact of the gall midge on biomass and these latter species remains unclear. seed production, but little about its biology, parasites, interac- Some gall midges of grasses directly impact seed production tions with other , or the interaction of the insect without seeming to affect vegetative biomass yield. For exam- with its host plant. Therefore, our primary goals were to ple, larvae of bluestem seed midge feed on the developing increase knowledge of the biology of the switchgrass gall caryopses and reduce seed yield of big bluestem. The larvae midge by determining (a) the seasonal occurrence of the of the bromegrass seed midge feed in the florets, consuming the different stages of its life cycle under field conditions, (b) ovary and stunting development of the stamens [18]. the duration of adult presence, (c) the overwintering condi- Stenodiplosis geniculati (Reuter) feeds on immature spikelets tions and life stage, and (d) rear and identify associated of creeping foxtail (Alopecurus arundinaceus Poir) in South parasitoids. Secondary goals were to (a) study the behavior Dakota [12, 19]. But, none of these appear to have an effect on of the switchgrass gall midge under field conditions and (b) vegetative growth [16, 20]. In contrast, the switchgrass gall determine if there were differences among three phenologi- midge has a direct negative impact on both seed and bio- cally distinct switchgrass cultivars for level of infestation. mass yield due to feeding at the apical internode. This Results of this study will be useful for the detection and feeding apparently interrupts the movement of photosynthates determination of the potential impact of the gall midge in the to the inflorescences, thus preventing caryopsis formation field. Also, understanding its phenology and life stages and and seed yield. accurate detection of symptoms of infestation will be impor- In general, larvae of most Chilophaga species have similar tant to switchgrass producers, agronomists, entomologists, feeding site behaviors. Larvae of Chilophaga gyrantis Gagné switchgrass breeders, or others involved in optimizing seed feed at the base of leaf sheaths and cause stem galls on and biomass yields of switchgrass. Aristida gyrans Chapman in Florida [16, 21]. Similarly, larvae of Chilophaga tripsaci (Felt) live inside sheaths and cause stem galls on Tripsacum dactyloides (L.), and larvae of Materials and Methods Chilophaga colorati (Felt) live at the base of a leaf sheath in a Muhlenbergia sp. [12, 16]. Larvae of a Chilophaga sp. Study Area This research was conducted at the South Dakota cause shortened internodes with tightly imbricated leaves in State University Research Farm, located at 44°15′14″Nand Bioenerg. Res. (2014) 7:417–423 419

96°40′17″W near Aurora, Brookings Co., South Dakota, dur- Larval Counts Field symptoms of infested tillers are primarily ing 2011 and 2012. The experimental area is composed of malformed inflorescences and premature dryness of the inflo- biomass production trials of commercial cultivars and spaced- rescences and the blade of the flag leaf. In 2011, 21 symptom- plant nurseries of experimental breeding populations of atic tillers were collected on 14 August and 25 tillers were switchgrass; cultivars evaluated in this study were collected on 29 September. In 2012, four tillers were collected ‘Dacotah’, ‘Sunburst’,and‘Cave-In-Rock’. These cultivars on 16 August, and seven tillers were collected on 29 August. are commonly grown for forage, conservation, and wildlife in Infested tillers were dissected in the lab for determination of this region. Nurseries were burned during mid-May during number of larvae per infested tiller, developmental stage, and 2011 and 2012 to remove unharvested plant residues. Data presence of parasitoids. were obtained during early May to December during 2011 and early April to late December 2012. The methods of observa- Infestation Rates Tillers infested by gall midge larva (Fig. 1) tion and sampling are described below. were observed during the growing season for time of emer- gence and general behavior of the adult and presence of Adult Emergence Gagné [12] suggested rearing gall midges in parasitoids during 2012. On 15 August 2012, numbers of pots filled with soil and sand, with peat moss atop, and placed in a infested tillers per square meter were counted for spaced cardboard shoebox, which had small holes that led to 8–10 dram plants (0.9 m centers) of ‘Dacotah’, ‘Sunburst’,and‘Cave- vials, which serve as traps for emergent adults. On 3 November In-Rock’ in a nursery composed of 37, 60, and 49 plants of 2011, eight cylindrical containers made from wire mesh (unit size each cultivar, respectively. Differences among the three culti- of the mesh wire 3×3 mm), 6.5 cm in diameter (54 units on mesh vars for infested tillers per square meter were determined by wire length) by 7 cm high (20 units on mesh wire), were filled using the linear model procedure for a completely randomized with soil, sampled from the upper 5 cm from a replicated biomass design in Statistix 9[27]. Fisher’s LSD was used to compare yield trial composed of seeded plots of 14 cultivars of switchgrass cultivar means at p <0.05. with varying symptoms of infestation by the gall midge. Affected sections of 10 infested tillers containing mature larvae were Parasitoid Rearing Wasps of Platygastridae [22]and placed on the surface of the soil in the cylinder. The exposed Eulophidae (Hymenoptera) were reared from larvae of the surfacewascoveredwithblackmeshfabricandtiedtoclose. gall midge in the lab at room temperature during the summer These containers were buried with the top at ground level in the of 2012. For rearing affected areas of several infested tillers field until spring or after snowmelt. Samples were taken period- containing parasitized larvae of the gall midge were rolled ically through April, May, or early June 2012. Tillers infested by the gall midge larva were collected in the field and observed in the lab during late June and July 2012.

Overwintering Stage Neiman and Manglitz [15] collected samples of soil from smooth bromegrass fields to determine the overwintering stage of the bromegrass seed midge in Nebraska. Our observations of the presence of fully grown larvae (i.e., late instar larva or mature larva) in infested tillers led us to question if the harboring region inside the sheath of the flag leaf came into contact with the soil would larvae migrate to the soil to overwinter? Therefore, on 10 May 2011, 18 samples of soil to a depth of about 3 cm were randomly collected over an area of about 100 m2. The area was spaced plants (0.81 m2 centers) of ‘Sunburst’ that we observed to be infested. For each sample, about 400 g of soil were collected using a garden trowel. The soil was sieved and washed through a series of three soil screens (US Standard Sieve Series: sieve nos. 12, 18, and 170). Larvae of the gall midge remained on the surface of the sieve no. 170 and were easily seen because of their bright orange color. They were collected into 80 % ethanol. Further, several inflorescences of infested tillers in the field were cov- ered with translucent organza cloth on 12 August 2011 to determine if the larvae overwintered while enclosed in the Fig. 1 Infested switchgrass (Dacotah) tiller demonstrating typical symp- sheath of the flag leaf. toms of switchgrass gall midge infestation (photo by V. Calles Torrez) 420 Bioenerg. Res. (2014) 7:417–423 with brown paper towels and placed in eight dram vials or was dull orange changing to bright orange by the last instar placed between layers of tissue paper in petri dishes. Distilled (Fig. 2b). Puparia were observed in infested tillers by mid- water was added as needed to provide humidity for the devel- July, and by 9 July, the first of the later emerging adults were oping parasitoids. Emergent adult wasps were provided a collected by sweeping. Adults were collected through 26 July solution of brown sugar and water in order to determine their (2.9 mm length averaged). longevity at room temperature. Infested tillers containing first instar larva on 21 June were collected on 10 July and taken to the lab. On 11 July, five adults emerged. These teneral individuals were fully colored within 24 h (Fig. 2d). We only occasionally collected adults by Results net sweeping from 9 July through late July. In addition, in tillers of ‘Cave-In-Rock’, we observed gall midge larvae, Emergence of Adults and Duration of Larvae On 12 April including some parasitized by P. chilophagae [22]. Also, clear 2012 and 12 May 2012, containers that were buried the empty puparia of the gall midge were observed, indicating previous autumn were recovered and tillers were dissected adult emergence in mid-July. By 16 August, larvae of the gall (one container for each excavation). At that time, larvae were midge were no longer observed in tillers of ‘Dacotah’. developmentally similar to the stage during the previous au- However, late instar larvae (Fig. 2b) were found feeding tumn (Fig. 2b). On 22 May, some larvae began forming brown within the sheaths of flag leaves in late summer through colored puparia (Fig. 2c) with a puparium length average of autumn in ‘Sunburst’ and ‘Cave-In-Rock’ during 2011 and 4.7 mm, and on 29 May, some had become pupae. By 31 May, 2012. In addition, overwintered late instar larvae (averaged of some pupae were turning orange color and had black bands on 4.8 mm in length) were observed in standing dead tillers the abdominal dorsum. Early June marked peak emergence of during mid-spring of 2012 and 2013. the early emerging adults (Fig. 2d). In late June, first instar larvae (Fig. 2a) were found in Overwintering Stage, Larvae, and Behavior under Field ‘Dacotah’, an early flowering upland cultivar selected from a Conditions Larvae of gall midge are gregarious. We found natural population near Bismarck, ND [26, 28]. First instar no evidence for cannibalism, and most individuals survived larvae were small (from 1.5 to 2.5 mm in length) and translu- winter in their groups within the sheath of the flag leaf of cent white (Fig. 2a), while body color in subsequent instars reproductive tillers (Fig. 2b). Mean number of larvae was

Fig. 2 Immature and adult stages of the switchgrass gall midge (scale bars=1 mm). a First instar larvae in culm (photo by V. Calles Torrez), b late instar larvae in culm (photo by P. Johnson), c puparium (photo by V. Calles Torrez), and d adult switchgrass gall midge (photo by P. Johnson) Bioenerg. Res. (2014) 7:417–423 421

31±2.4 (n =57 tillers) with a range from 6 to 85 per infested emerged from gall midge larvae on 17 July in the lab 8 days tiller. Full-grown larvae overwintered and adults emerged after the collection of infested tillers, then eight adults emerged from standing infested tillers, prostrate wind-blown infested on 23 July after 5 days of infested tillers collected, and three tillers, or within the top 2.5 cm of the soil. In standing tillers, adults emerged in 26 July after 3 days. Seven adults were adults (Fig. 2d) emerged by crawling to the distal end of the collected in the field from an infested tiller that was covered partially enclosed panicle and escaping through gaps. with white organza on 23 July, and in the same day, eight adults Eclosion and adult emergence were observed to occur in the emerged in the lab. Adults emerged from small exit holes morning. Adults lived from 2 to 3 days in the lab when brown (Fig. 3a) of their making by chewing in the gall midge infested sugar water was provided. section of the infested tiller. Specimens were also collected by net sweeping until late July. The cocoon of Quadrastichus sp. Infestation Rates for Three Phenologically Distinct is brown colored (Fig. 3a), and the immature adult inside the Cultivars Highly significant differences (p <0.01) were found cocoon is pale orange-yellow similar to the color of the ab- among cultivars for number of infested tillers per square dominal venter of the wasp adult. One Quadrastichus sp. meter. ‘Cave-In-Rock’, the latest flowering of the three culti- emerged from each gall midge larva parasitized with about vars with anthesis beginning on 12 August, had the highest eight gall midge larvae parasitized per infested tiller. The number of infested tillers per square meter, which was >2× Quadrastichus sp. adults (Fig. 3b) remained alive more than that for ‘Dacotah’. ‘Dacotah’ entered anthesis on 8 July and 30 days when fed with a solution of brown sugar and water in had the fewest infested tillers per square meter. ‘Sunburst’ the lab. The empty puparium of the gall midge is easy to averaged 17 infested tillers per square meter and started an- distinguish from the brown cocoon of the parasitoid because thesis on 28 July (Table 1). In general, infested tillers (Fig. 1) of its translucent white coloration and texture. were smaller with malformed inflorescences that produced no mature seed and were partially encased in the sheath of the flag leaf as described by Boe and Gagné [11]. In addition, they Discussion reported that the mean weight of infested tillers was 35 % less than healthy tillers, indicating that this infestation level would In the field, the time between the initiation of pupation to the cause an impact on biomass production. Tiller-based estimates adult of the gall midge is approximately 10 days. Boe and are reasonable predictors of biomass loss [29] as there is no Gagné [11] reported the beginning of pupation by 2 May with compensatory growth by switchgrass following tiller loss and adult emergence beginning by 17 May, giving nine pupal days no significant mid to late season tiller additions to a plant. under lab conditions. In this study, early emergence was later (early June) in the field. Gagné [12] pointed out that humidity and temperature play important roles in timing of adult emer- gence of cecidomyiid species using the life cycle and activities Parasitoids Associated with Switchgrass Gall Midge of Sitodiplosis mosella (Géhin) as an example [30]. Also, moisture content of the soil, regardless of soil types, had a The recently discovered [22] parasitoid P.chilophagae was significant effect on the emergence of nasturtii reared from late instar larvae of the gall midge in our lab (Kieffer) [31]. and collected in the field. This wasp appears to be the Larvae of the gall midge spend nearly 10 months of the primary parasitoid of C. virgati. In addition, four adults of a calendar year enclosed in the sheath of the flag leaf from late Quadrastichus sp. (Hymenoptera: Eulophidae: Tetrastichinae) summer through mid-spring of the following year. The early emergence of adults of the gall midge in early June and a later emergence in mid-July suggests a bivoltine (two generations Ta b l e 1 Means and ranges for number of infested tiller per square meter per year) behavior in eastern South Dakota. Similarly, the for three cultivars of switchgrass with different phenologies by the clover-flower midge, Dasyneura leguminicola (Lintner), that switchgrass gall midge at Brookings, SD, USA, during 2012 overwinters as a larva and the adults emerge from the soil Cultivar n Mean infested Minimum and Date of during April and May. Females oviposit on young red clover − tillers (m 2) maximum infested anthesis (Trifolium pratense L.) inflorescences, and larvae pupate in −2 tillers (m ) the soil emerge as a second generation during early July [32]. Dacotah 37 11 4–26 July 8 Also, Stenodiplosis wattsi has at least three generations per Sunburst 60 17 2–63 July 28 year [33], and S. bromicola has two generations per year [15]. Cave-In-Rock 49 27 4–96 August 12 Thus, multivoltinism appears to be common in forb and grass- feeding gall midges. LSD (0.05) 5.7 Alternatively, we wonder if the late emergence (i.e., puta- n number of plants tive second generation in July) of the adult of gall midge was 422 Bioenerg. Res. (2014) 7:417–423

Fig. 3 a Remnant gall midge puparia (lower) and exit holes (upper)madebyadult Quadrastichus sp. in a switchgrass tiller; b a freshly emerged adult Quadrastichus sp. (scale bars=1 mm) (photos by V. Calles Torrez)

in response to the timing of the natural tiller senescence in burning or spring grazing by cattle could reduce the popula- ‘Dacotah’, which was selected from indigenous populations tion of the midge in the harvested area. However, the appli- of switchgrass and matures a month earlier than ‘Sunburst’.A cation of fire or grazing, or harvest for other than biomass, is similar pattern occurs for the first generation of S. bromicola counter to the desire to produce biomass feedstock material. in bromegrass, which emerges in response to the physiological Such methods may not be effective as well due to the presence maturity of bromegrass [15]. In the two later maturing culti- of overwintering larvae in the soil. Whether or not the adults vars, ‘Sunburst’ which is indigenous to eastern South Dakota of the midge could emerge from baled switchgrass remains and ‘Cave-In-Rock’ which is native to southern Illinois ma- unknown. If the switchgrass is harvested for seed, the ture 2 weeks later than ‘Sunburst’ [26, 28] in which the larvae overwintering larvae could be collected with the grain and of the gall midge overwintered. Whether or not these transported or blown out the back of a combine harvester with overwintering larvae are actually the progeny of second gen- light organic fraction. The latter possibility was observed eration adult reared from ‘Dacotah’ or from first generation during seed harvest of ‘Sunburst’ and ‘Nebraska 28’ (Fig. 4) adults is unknown. However, no larvae were observed in at EcoSun Prairie Farm near Colman, SD, during October tillers of ‘Dacotah’ after August. Whether or not this is 2012. The bright orange late instar larvae were conspicuous bivoltine behavior, the gall midge had two periods of emer- in the harvested switchgrass seed in the grain bin of the gence of adults per year in switchgrass stands composed of combine harvester, but we are unaware of any effective meth- three phenologically distinct cultivars. Gagné [12]indicated od that could separate the larvae from the seed during harvest, midges have flexible behavior and respond to variation in though no larvae were detected in well cleaned and bagged climatic conditions. He also noted that plant-feeding adult gall seed. We could expect population density to be seasonally midges have short lifespans. The adults of the switchgrass gall reduced under management for biomass or seed production. midge survived 2 or 3 days in the lab in this study, which is a Based on our observations, the density of local popu- longer lifespan than for females of Contarinia sorghicola lations of the gall midge is related to the available in (Coquillett) that live less than 1 day [34]. standing switchgrass in the vicinity. In the northern Great Infestation by the larvae of the gall midge causes stunting Plains, in addition to forage and seed production plantings, of the apical tiller internodes and premature death of the switchgrass occurs in roadside, conservation and inflorescence in switchgrass [11]. This malformation causes negative impacts on biomass and seed production. The wide variation in numbers of larvae per infested tiller especially lower numbers suggest that parasitoids may have an influence, as similarly suggested by Tokuda [24] for gall midges in the tribe Asphondyliini. So far, we have reared and identified two parasitoids from the switchgrass gall midge. Of the two spe- cies of parasitoid collected during this study, P. chilophagae is a polyembryonic species [22], whereas single adults of the Quadrastichus sp. emerged from individual gall midge larva. Further work is needed to determine the biological control potential of these parasitoids to benefit seed and biomass yield of switchgrass. Since a high percentage of the switchgrass gall midge larvae overwinter in standing reproductive tillers, it seems Fig. 4 Late instar larvae of the switchgrass gall midge among seeds of reasonable to expect that removing the standing crop during switchgrass in a grain bin sample from combine harvester during seed autumn for biofuel, hay, bedding, or other purposes or by field harvest (photo by P. Johnson) Bioenerg. Res. (2014) 7:417–423 423 ornamental plantings, native prairies, and wildlife areas. 13. Gagné RJ (2004) A catalog of the Cecidomyiidae (Diptera) of the However, how far the adults of the switchgrass gall midge world. Memoirs Entomol Soc Wash 23:408 14. Barnes HF (1931) Gall midges (Cecidomyiidae) whose larvae pre- can move by flight or wind remains unknown. In one ancillary vent seed production in grasses (Gramineae). Bull Ent Res 22: study, we noted the occurrence of the gall midge in the second 199–203 summer after planting when known switchgrass was more 15. Neiman EL, Manglitz GR (1972) The biology and ecology of the than 0.25 miles distant. Thus, effectiveness of aforementioned bromegrass seed midge in Nebraska. Res Bull 252 16. Gagné RJ (2010) Update for a catalog of the Cecidomyiidae (Diptera) management practices would be if populations of the gall of the world. Digital version 1. http://www.ars.usda.gov/ midge occurred in nearby conservation or other unmanaged SP2UserFiles/Place/12754100/Gagne_2010_World_Catalog_ stands is also unknown. Cecidomyiidae.pdf.Accessed18June2013 17. Boe A, Keeler KH, Normann GA, Hatch SL (2004) Switchgrass. In: Moser LE (ed) The indigenous bluestems of the western hemisphere Acknowledgments The US Department of Energy and the North- and gambagrass. Agron Monogr 45 ASA, Madison, pp 873–908 Central Sun Grant Program are thanked for their support. This work 18. Vogel KP, Manglitz GR (1989) Bluestem seed midge influence on was done primarily at the Insect Biodiversity Lab, Plant Science Depart- sexual reproduction of big bluestem: a review. Proceedings of the ment, South Dakota State University. Dr. Nels Troelstrup is thanked for Eleventh North American Prairie Conference, pp 267–270 allowing additional studies at the Oak Lake Field Station, South Dakota 19. Boe A (1991) A new host record for Contarinia geniculati (Reuter) State University, in northeastern Brookings County, SD. (Diptera: Cecidomyiidae). Proc Entomol Soc Wash 93:789 20. Boe A, Robbins K, McDaniel B (1989) Spikelet characteristics and midge predation of hermaphroditic genotypes of big bluestem. Crop References Sci 29:1433–1435 21. Gagné RJ, Stegmaier CE Jr (1971) A new species of Chilophaga on Aristida (Graminea) in Florida (Diptera: Cecidomyiidae). Florida 1. Parrish JD, Casler MD, Monti A (2012) Switchgrass a valuable Entomol Soc 54:335–338 biomass crop for energy. In: Monti A (ed) The evolution of switch- 22. Johnson PJ, Buhl PN, Calles Torrez V (2013) A new species of grass as an energy crop. Springer, London, pp 1–28 Platygaster (Hymenoptera: Platygastridae) parasitizing Chilophaga – 2. Vogel KP (2004) Switchgrass. In: Moser LE (ed) Warm-Season (C4) Vi rg a t i Gagné (Diptera: Cecidomyiidae). Zootaxa 3630(1):184 190 Grasses. Agron Monogr 45 ASA, Madison, pp 561–588 23. Yukawa J (1983) community centred upon the Neolitsea 3. McLaughlin SB, Walsh ME (1998) Evaluating environmental con- leaf gall midge, Pseudasphondylia neolitseae Yukawa (Diptera, sequences of producing herbaceous crops for bioenergy. Biomass Cecidomyiidae) and its host plant, Neolitsea sericea (Blume) Koidz. Bioenergy 14:317–324 (Lauraceae). Menoris Fac Agr Kagoshima Univ Repository 19:89–96 4. Murray LD, Best LB (2003) Short-Term bird response to harvesting 24. Tokuda M (2012) Biology of Asphondyliini (Diptera: Cecidomyiidae). switchgrass for biomass in Iowa. J Wildl Manage 67:611–621 Entomol Sci 15:361–383 5. Gustafson DM, Boe A, Jin Y (2003) Genetic variation for Puccinia 25. Berdahl JD, Frank AB, Krupinsky JM, Carr PM, Hanson JD, Johnson emaculata infection in switchgrass. Crop Sci 43:755–759 HA (2005) Biomass yield, phenology, and survival of diverse switch- 6. Metzler EH, Shuey JA, Ferge LA, Henderson RA, Goldstein PZ grass cultivars and experimental strains in western North Dakota. (2005) Contributions to the understanding of tallgrass prairie- Agron J 97:549–555 dependent butterflies and moths (Lepidoptera) and their biogeogra- 26. Lee DK, Boe A (2005) Biomass production of switchgrass in Central phy in the United States. Ohio Biol Surv 15(1):143 South Dakota. Crop Sci 45:2583–2590 7. Adamski D, Johnson PJ, Boe AA, Bradshaw JD, Pultyniewicz A (2010) 27. Software A (2008) Statistix 9 user's manual. Analytical Software, Descriptions of life-stages of Blastobasis repartella (Lepidoptera: Tallahassee Gelechioidea: Coleophoridae: Blastobasinae) and observation on its 28. Zegada-Lizarazu W, Wullschleger SD, Surendran Nair S, Monti A biology in switchgrass. Zootaxa 2656:41–54 (2012) Switchgrass a valuable biomass crop for energy. In: Monti A 8. Schaeffer S, Baxendale F, Heng-Moss T, Sitz R, Sarath G, Mitchell (ed) Crop Physiology. Springer, London, pp 55–86 RB, Shearman R (2011) Litter accumulation and decomposition in 29. Thomsen PM, Brummer EC, Shriver J, Munkvold GP (2008) Bio- pastures. In: Guretzky J (ed) The arthropod community associated mass yield reductions in switchgrass due to smut caused by Tilletia with switchgrass in Nebraska. Department of Agronomy and Horti- maclaganii. http://www.plantmanagementnetwork.org/pub/php/ culture, University of Nebraska-Lincoln, 17 (2) research/2008/smut/. Accessed 18 June 2013 9. Calles Torrez V,Johnson PJ, Boe A (2013) Infestation Rates and tiller 30. Knodel J, Ganehiarachchi M (2008) Integrated pest management of the morphology effects by the switchgrass moth on six cultivars of wheat midge in North Dakota. North Dakota State University E-1330 switchgrass. Bioenerg Res 6:808–812 31. Chen M, Shelton AM (2007) Impact of soil type, moisture, and depth 10. Prasifka JR, Bradshaw LD, Boe AA, Lee DK, Adamski D, Gray ME on Swede midge (Diptera: Cecidomyiidae) pupation and emergence. (2010) Symptoms, distribution and abundance of the stem-boring Environ Entomol 36:1349–1355 caterpillar, Blastobasis repartella (Dietz), in switchgrass. Bioenergy 32. Creel CW, Rockwood LP (1947) The control of the clover-flower Res 3:238–242 midge. USDA, Farmer's Bull No 971 11. Boe A, Gagné RJ (2011) A new species of gall midge (Diptera: 33. Carter MR, Manglitz GR, Rethwish MD, Vogel KP (1988) A seed Cecidomyiidae) infesting switchgrass in the Northern Great Plains. midge pest of big bluestem. J Range Manage 41(3):253–254 Bioenergy Res 4:77–84 34. Waquil JM, Teetes GL, Peterson GC (1986) Sorghum midge (Diptera: 12. Gagné RJ (1989) The plant-feeding gall midges of North America. Cecidomyiidae) adult ovipositional behavior on resistant and suscep- Cornell University, Ithaca tible sorghum hybrids. J Econ Entomol 79:530–532