BOLETIN DEL MUSEO ENTOMOLÓGICO FRANCISCO LUÍS GALLEGO

ARTÍCULO DE OPINIÓN

ENTOMOLOGICAL DISCOVERIES IN THE DOMESTICATION OF NATIVE PRAIRIE PLANTS

Paul J. Johnson, Ph.D.

Insect Biodiversity Laboratory and Severin-McDaniel Research Collection, South Dakota State University, Brookings, South Dakota, U.S.A. e-mail: [email protected]

Certain native grasses and one dicot are currently being investigated at South Dakota State University for their value and potential as biomass feedstock for the production of cellulose- derived ethanol. The expectation is that these plants will be grown on croplands that are least productive for maize, soybean, or wheat, and are typically highly erodible, are conservation lands, or are otherwise not optimum for most crops. Not surprisingly, each of these native plants have associated with them, but the involved and their relationships to their host plants are poorly understood and their dynamics are only now being investigated as the plants are brought into monocultural agronomic production.

This presentation will review several species of insects that are now regarded as significant pests of native plants being investigated as biomass feedstock crops. The discovery of these insects and the nature of their relationships with their host plants provide superior examples and models that illustrate the need and value of in-depth life cycle investigations, and also illustrate that new species and life styles continue to be discoverable by simply looking closer at native and agroecosystem biodiversity.

Our research team involves four principal investigators and four additional collaborators. I am the senior P.I. (principal investigator) entomologist and project leader, with a joint

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appointment in the departments of Plant Four basic entomological goals Sciences (PS) and Natural Resource define our studies on these insect- Management (NRM). My co-PI’s are plant relationships: 1) Complete our Dr. Susan Rupp (Dept. NRM), a wildlife understanding of the life stages of specialist studying small mammals and each potential pest species, to include birds; Dr. Arvid Boe (Dept. PS), a native elucidating their ; describing plants agronomist and breeder; and Dr. as needed each life stage, characterize Vance Owens (Dept. PS), a forages and each life stage periodicity, duration, and biomass production agronomist. microhabitats; acertain their dynamic relationship to their host phenology; Three species of grass (Poaceae) are the and assess the identity and activity focus of our studies, namely Switchgrass of cellulases in the larval guts of (Panicum virgatum), Prairie cordgrass each species. 2) Estimate population (Spartina pectinata), and Big bluestem development rates, density, and (Andropogon gerardii). The dicot is Cup abundance. 3) Determine the presence, plant (), a large identity, and phenology of parasites statured species of the Asteraceae. and predators. 4) Quantify plant The grasses are intended to form the development and biomass changes foundation of each agroecosystem resulting from insect feeding in the community with specific proportions different life stages. All studies are being tailored for the field site and condition conducted at two research farm and two as each species has differing tolerances native community sites in eastern South to soil conditions and moisture Dakota that are within the natural range demands. Cup plant is intended as a of the host plants in the Tallgrass Prairie complementary and compatible species Biome. These sites are the Oak Lake that will grow with the grasses, provides Field Station, Aurora Research Farm, Felt considerable additive biomass, and can Research Farm, and Aurora Prairie, all be grown and harvested in concert with within 25 miles distance of Brookings, the grasses. The Cup plant also adds to South Dakota. the agroecosystem as a species highly attractive to a wide diversity of pollinators. Switchgass, Panicum virgatum Other native species will also be planted in fields to provide biodiversity, though Switchgrass is a native, medium to tall they would be negligible for significant (≤ ca. 2 m), warm-season, bunch grass additional biomass. Each plant species found throughout most of North America being studied has several insect species except the far western provinces and identified as potentially significant pests states of Canada and the United States. in agronomic plantings, some of which This is a perennial species that occurs remain undetermined and at least one in a diversity of habitats with mesic (Switchgrass midge) was discovered soils, including prairies, meadows, as an undescribed species. Here, I will and ruderal sites, and is co-dominant focus on some of the insects associated with Sorghastrum nutans, Schizachyrium with Panicum virgatum and Silphium scoparium, and Andropogon gerardii. perfoliatum. Switchgrass provides high value food and cover for wildlife, imported game

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birds, and is used extensively for erosion third leaf stage. Pupation occurs in the prevention and conservation plantings, tiller in late June and early July. We did and it has a massive root system that rear a parasitoid from the pupa, sequesters high quantities of carbon. the wasp Bassus difficilis Muesebeck Due to its native status and high biomass (Hymenoptera: Braconidae). productivity it is highly ranked as a potential crop for biomass feedstock The impact of this moth on Switchgrass is and ethanol production. highly variable, but typically significant. In wild plant populations the immature Three insects, two and one fly, have stages are nearly impossible to find and shown themselves as significant pests effects on the plant extremely difficult to of Switchgrass. None of these species assess. However, in agronomic conditions were associated with Switchgrass prior this insect can be very abundant at to recent studies. The Switchgrass times resulting in upwards of 40% of moth, Blastobasis repartella (Dietz) tillers being damaged per plant and first had its biology summarized by a 5-10% range of infestation being (Adamski et al. 2010). The Switchgrass typical, giving an arithmetic estimate of midge, Chilophaga virgati Gagné, was 750,000 larvae/ha. All occupied tillers described (Boe and Gagné 2011) from die prematurely, giving a loss of biomass specimens discovered during this study. and seed production. Meanwhile, the so-called Top-node borer (: Crambidae), remains During investigation on the Switchgrass unidentified at the genus and species moth, it was found that inflorescences levels. of Switchgrass were not developing normally and prematurely died. Based Blastobasis repartella was first collected on previous experience with a gall midge by two specimens in 1906 at Denver, (Diptera: Cecidomyiidae) in Andopogon Colorado, using an electric light, which gerardii, team member Dr. Arvid Boe at that time what was a novel technique suspected a midge in Switchgrass. for collecting insects, and was then Larvae of a midge were found at the base described it in 1910. The types found of each senescing inflorescence from their way to the U.S. National Museum July through August where they feed of Natural History, but as a small (< 10 in the intercalary meristem area at the mm long) grey-white moth the species base of the peduncle. Through rearing remained essentially unknown until 2008 it was found that a new species of gall when I reared and collected specimens midge was responsible, and as noted from Switchgrass grown near Brookings, earlier this was described as Chilophaga South Dakota. Now, the species is known virgati. The larvae remain in the damaged from seven States. The adult is active in tiller until autumn when they start to July and August, the female lays eggs drop from the tiller and burrow into the at the base of the tiller, and the larvae soil for a winter-long dormancy. They overwinter and feed in the proaxis of the remain as larvae into mid-spring and rhizome. In early spring the larvae extend then pupate when the host plants begin feeding into the basal internodes of new their seasonal growth. Though we do not tillers and kill them before reaching the yet know where the eggs are deposited,

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they must be laid when the host tillers system that sequesters high quantities are growing actively in June. of carbon. Due to its native status and high biomass productivity it is highly Plants infested by C. virgati lose biomass ranked as a potential crop to interplant upwards of 35% below production of with grasses for biomass feedstock uninfested tillers. Since the damage and ethanol production. Relatively few prevents normal inflorescence insects feed on Cup plant, but those development then there is also a 100% that do have some most interesting life loss of seed production from infested cycles. tillers. There is a tolerance differential by cultivar ranging from 7.2-21.8%, giganteana (Lepidoptera: suggesting that resistance breeding may Torticidae) is the largest tortricid moth be possible. in North America and is associated only with Silphium spp. (Asteraceae). The The third insect in Switchgrass is adults are active from early July through another moth of the Family Crambidae. mid-August and are mimics of bird feces Thus far we have several instars of the that are abundant on the host plant larva, which bore through the terminal leaves. Eggs are laid primarily in early two internodes of nearly mature and mid July when the stems are bolting tillers. Unfortunately, we have yet to and the first instar larvae commence successfully rear this species, so we do feeding on the developing disc and ray not yet have a confirmed identification. flowers. Second and third instar larvae It appears that the larva of this species burrow into the buds and feed internally drops from the plant at maturity in late on all floral parts, including the August and probably pupates in soil at hypanthium and ovaries, and ultimately the base of plants. We expect that the kill the buds. By late August and early insect over-winters either as a dormant September the larvae leave the dead mature larva or as a pupa, with the adult inflorescences and move through the soil emerging in late spring. and along emergent stems to the crown area where they begin feeding and enter Cup plant, Silphium perfoliatum the rhizome. Mature larvae overwinter in the, excavating large chambers in Cup plant is a native, warm-season, the vascular and parenchymal tissues medium to tall (≤ 2.5 m) flowering that become infected with fungi and plant found throughout most of eastern bacteria. At some point in spring the boreal North America east of the Rocky larvae leave the rhizome and pupate, Mountains. This is a perennial species probably in the surrounding soil. Pupal that occurs mostly in lowland habitats exuviae attributed to this species can be with strongly mesic soils, including found partially emergent from the soil at streamsides, wetland margins, and the plant base in late June. vernal wet meadows. Cup plant provides high value food for wildlife, including Wild populations of S. perfoliatum have a wide diversity of pollinators, and relatively low incidences of infestation, is used extensively for conservation with typically <10% of buds infested plantings. This plant has a massive root and killed by early instar larvae. In

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contrast, agronomic populations suffer In the search for ecological appropriate considerable loss with 95-100% of floral and environmental adaptable plants and seed crops annually. Multiple years for biomass production in the Upper of infestation have the plants losing Midwest and northern Great Plains vigor within 3 years resulting in 50-70% native plants are being studied. This loss of biomass in addition to the floral shift in plant as crops brings a wealth damage. of native species associates that are often poorly known or even undescribed Uroleucon cf. ambrosiae is a curious aphid species. The examples given here of that is similar to Uroleucon populations insect associates of switchgrass and on Ambrosia spp. Populations of U. cf. cup plant demonstrate this trend and ambrosiae on S. perfoliatum can become illustrate that these insects also possess large and dense, being found on leaves, unusual life histories that are biologically peduncles, stems, and floral parts. intriguing. These examples plainly This aphid is inconstant on Cup plant, demonstrate the wealth of investigatory geographically and temporally, and potential in biology using relatively low- has short-lived colonies that develop cost technology and high value field and crash within 4-6 weeks, but still techniques and curiosity. As a side attract large numbers of predators benefit, rational agronomic protocols and parasitoids, including lacewings can be developed early in the cropping (Neuroptera: Chrysopidae, Chrysoperla evolution of plants when the natural plorabunda), ladybeetles (Coleoptera: history of the plants and their insect Coccinellidae, Hippodamia convergens), associates are properly elucidated. flower flies (Diptera: Syrphidae), and a parasitoid wasp (Hymenoptera: Acknowledgements Braconidae, Acanthocaudus n.sp.). To date, we have not found any evidence The North Central Regional Sun Grant of virus transmission or discernable Center at South Dakota State University damage from feeding, other than slight through a grant from the US Department chlorosis at sites of denser colonies. The of Energy Biomass Feedstock Production Acanthocaudus n.sp. parasitoid helps Program has supported research on the illustrate a common modern malady switchgrass moth and midge. The Burris when working with alternative crops. The McDaniel Insect Collection Endowment, type locality of this new wasp was part SDSU Agricultural Experiment Station, of an agronomy research farm on the Oak Lake Field Station, EcoSun South Dakota State University campus, Prairie Farms, Inc., and the SD Crop but was destroyed to construct an access Improvement Association provided road for a business development. funding and access to experimental plots and fields. Summary References A curious historical trend in the United States and many other countries is to Adamski D, Johnson PJ, Boe A, Bradshaw extensively use non-native plants for J, Pultyniewicz A. 2010. Descriptions crops, particularly as food or fuel plants. of life-stages of Blastobasis repartella

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(Lepidoptera: Gelechioidea: Coleophoridae: Blastobasinae) and observations on its biology in switchgrass. Zootaxa. 2656: 41-54.

Boe A, Gagné RJ. 2011. A new species of gall midge (Diptera: Cecidomyiidae) infesting switchgrass in the northern Great Plains. BioEnergy Research. 4(2): 77-84.

Blastobasis repartella, larva in proaxis

Panicum virgatum

Chilophaga virgati, larvae in stem

Blastobasis repartella, adult Chilophaga virgati, adult

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Silphium perfoliatum, inflorescence Eucosma giganteana, mature larva

Silphium perfoliatum, root mass Uroleucon cf.ambrosiae

Acanthocaudus n.sp.

Eucosma giganteana, adult

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