The Southern Cornstalk Borer (Diatraea crambidoides (Grote), Lepidoptera: Crambidae) a New Pest of Eastern Gamagrass (Tripsacum dactyloides (L.) L., Poaceae)

The Southern Cornstalk Borer (Diatraea crambidoides (Grote), Lepidoptera: Crambidae) a New Pest of Eastern Gamagrass (Tripsacum dactyloides (L.) L., Poaceae) Author(s) :T. L. Springer, G. J. Puterka, D. L. Maas, and E. T. Thacker Source: Journal of the Kansas Entomological Society, 84(3):209-216. 2011. Published By: Kansas Entomological Society URL: http://www.bioone.org/doi/full/10.2317/JKES100907.1

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JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY 84(3), 2011, pp. 209–216

The Southern Cornstalk Borer (Diatraea crambidoides (Grote), Lepidoptera: Crambidae) a New Pest of Eastern Gamagrass (Tripsacum dactyloides (L.) L., Poaceae) T. L. SPRINGER,1 G. J. PUTERKA,2 D. L. MAAS,1,3

AND

E. T. THACKER1

ABSTRACT: The southern corn stalk borer [Diatraea crambidoides (Grote)] has become a serious pest to eastern gamagrass [Tripsacum dactyloides (L.) L.]. Managing this insect will be important to the future of this forage crop in the United States. An experiment was conducted to understand the life cycle of the southern corn stalk borer infesting eastern gamagrass. For a two year period, four plant crowns which contained numerous shoots were dug randomly each week from a field plot located in Woodward, OK. All shoots from each crown were dissected and the number of larvae and pupae present was recorded for each shoot type, i.e., reproductive or vegetative shoot. The life stages of the southern corn stalk borer in eastern gamagrass can be described by three distinct populations in northwestern Oklahoma: a) overwintering, b) first generation, and c) second generation. Over-wintering larvae feed within a cavity near the base of the shoot or within the proaxis. Pupation occurred within the feeding cavity. Larvae occurred in reproductive shoots 2.5 times more often than in the vegetative shoots, which suggested an oviposition preference by adult females for reproductive shoots. The life cycle of the southern corn stalk borer in eastern gamagrass was completed in about 911 cumulated growing degree days. Understanding the life cycle of this insect devastating to eastern gamagrass forage and seed production will help formulate methods of control. KEY WORDS: Southern corn stalk borer, life stages, populations, Oklahoma, degree days

The southern corn stalk borer [Diatraea crambidoides (Grote)], as its name implies, is an economic pest of corn, Zea mays L., throughout the southern USA from Maryland and Kansas on the north and southward into the southern and southwestern states. This pest also occurs in Mexico and in South America (Heinrichs et al., 2000). Southern corn stalk borer larvae tunnel and feed in the leaf whorls of corn creating irregular shaped holes in the leaves as they unfurl, tunnel in leaf mid-ribs, and tunnel and create cavities in the upper and lower corn stalk (Howard, 1891; Ainslie, 1919; Phillips et al., 1921; Cartwright, 1934). Corn plants will often out grow damage caused by low infestations of this insect; however, reduced grain and ensilage yields occur with moderate infestations, and plant death is often reported with high infestations (Heinrichs et al., 2000). Howard (1891) reported the host range of the southern corn stalk borer to include eastern gamagrass [Tripsacum dactyloides (L.) L.], and stated that, ‘‘The borer in this food plant introduces a variation in habit, and it feeds mainly on the upper joints, some larvae even having been found feeding upon the seed heads.’’ He reported that eastern gamagrass plants adjacent to a corn field were highly infested with southern corn stalk borer larvae while only one stalk of corn was found with borer damage. He further suggested that burning eastern gamagrass in the vicinity of corn fields 1 USDA, Agricultural Research Service, Southern Plains Range Research Station, 2000 18th Street, Woodward, Oklahoma 73801, USA. 2 USDA, Agricultural Research Service, Wheat, Peanut, and Other Field Crops Research Unit, 1301 N. Western Street, Stillwater, Oklahoma 74075, USA. 3 Current address: Monsanto, 800 North Lindbergh Blvd, St. Louis, Missouri 63141, USA.

Accepted 10 June 2011; Revised 23 August 2011

E 2011 Kansas Entomological Society

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every winter should reduce the number of hibernating individuals which would otherwise infest corn fields in the spring. Ainslie (1919) reported the host range to include sorghum [Sorghum bicolor (L.) Moench], Johnsongrass [Sorghum halepense (L.) Pers.], sugar cane (Saccharum officinarum L.), and eastern gamagrass. He stated that, ‘‘The injury to plants other than corn is never severe but, in planning methods of control, these plants must be considered and an examination made to determine whether or not they are harboring the pest.’’ Contrary to Ainslie (1919), Krizek et al. (2003) reported severe dieback to eastern gamagrass plants in research plots at the USDA-ARS Beltsville Agricultural Research Center, Beltsville, MD, in 2001 and consequently attributed the dieback to the southern corn stalk borer. They observed several larvae emerging from eastern gamagrass crowns. In April 2002, in field plots at the USDA-ARS Southern Plains Range Research Station, Woodward, OK and in pastures at the USDA-ARS Southern Plains Experimental Range near Ft. Supply, OK, southern corn stalk borer larvae and pupae were collected in the base of the prior year’s reproductive shoots and in the base of current year vegetative shoots of eastern gamagrass plant crowns (Springer et al., 2003; Maas and Springer, 2005). Maas and Springer (2005) did not observe the severe dieback to eastern gamagrass plants in Oklahoma that was reported by Krizek et al. (2003). However, Springer et al. (2004) estimated forage yield losses caused by the southern corn stalk borer to eastern gamagrass of as much as 1000 kg ha21, or economic losses of $50.00 per hectare for severely infested fields. Eastern gamagrass is a highly productive and palatable perennial, warm-season grass used for pasture, hay, and conservation purposes. Its breeding and agronomic potential and insect pest problems have been reviewed by Springer and Dewald (2004). As the number of hectares of eastern gamagrass increases in the United States (Springer and Dewald, 2004), the incidences of disease and insect pests have become more evident. Plant diseases and insects commonly found to occur in corn are now becoming prevalent in eastern gamagrass. Cultural practices used to control many of these insects in corn are not applicable to eastern gamagrass because it is grown as a perennial crop. Additionally, few chemical control measures are labeled for use on eastern gamagrass. The USDA-ARS Southern Plains Rangeland Research Station maintains the largest collection of temperate eastern gamagrass germplasm in the United States with more than 500 accessions. We have assessed our collection and found no resistance to the southern corn stalk borer. Eastern gamagrass, a close relative of maize, has been used as a genetic source for developing disease and insect resistant maize lines (Bergquist, 1981; de Wet, 1979; Moellenbeck et al., 1995). Maize lines with limited resistance to the southwestern corn borer [Diatraea grandiosella Dyar] are available. It is possible to transfer genes from maize into eastern gamagrass, but the process could require 10 years or more. Development of Bt gamagrass is another possible alternative (Krizek et al., 2003), but is unlikely due to regulatory issues. The utilization of eastern gamagrass for pasture, hay, and soil stabilization is increasing every year (Springer and Dewald, 2004). Other uses, such as pharmaceuticals and grain for human consumption or livestock feed, also are being explored. As the hectares of eastern gamagrass increase, it will be important to develop strategies to minimize the economic impact imposed on the crop by the southern corn stock borer and other pests. We anticipate that these problems will be solved through an

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integrated approach of plant breeding and cultural practices. Because knowledge of the life cycle of the southern corn stalk borer in eastern gamagrass will be useful for developing cultural practices for control, research was conducted to understand the life stages of development of the southern corn stalk borer in this host. Materials and Methods This experiment was conducted at the USDA-ARS Southern Plains Range Research Station, Woodward, OK (36u259N 99u249W, elevation 615 m). The field plot consisted of 1200 plants of eastern gamagrass germplasm ‘FGT-1’ (Dewald and Kindiger, 1996) which were transplanted from the greenhouse to the field in 1996. Plants were spaced in 1.1 m rows on 1.1 m centers within rows on Devol fine sandy loam (Coarse-loamy, mixed, superactive, thermic Typic Haplustalfs) soil. Each year after establishment, the plot was burned in mid-March and atrazine [2-chloro-4ethylamino-6-isopropylamino-s-triazine] was applied 7 to 14 days later for weed control at 1.68 kg of AI per hectare. The field plot was fertilized each year in April with nitrogen in the form of urea (46-0-0) at 70 kg N ha21. Beginning in January 2003 and continuing through December 2004, four plant crowns were dug randomly each week for a two-year period. Sampling was conducted on the east side of the field plot the first year of the experiment; sampling was conducted the second year on the north side of the field plot. Each year, the first row of the plot was designated a border row and all samples were taken by digging plants from rows 2–9. Sampling was conducted in this fashion to protect the integrity of the plot because it was used to maintain seed and vegetative propagules for the FGT-1 germplasm release. Each year, replicate 1 was sampled randomly from rows 2 and 3, replicate 2 was sampled randomly from rows 4 and 5, replicate 3 was sampled randomly from rows 6 and 7, and replicate 4 was sampled randomly from rows 8 and 9. For each week of the experiment, four plants (one from each replicate) were dug from the field plot, transported to a barn where each crown was hand-split into single and compound shoots (Dewald and Louthan, 1979), and then visually classified into reproductive or vegetative shoots. Pruning shears were used to cut each shoot transversely, beginning at the tip and proceeding down to the base, to determine presence or absence of southern corn stalk borer larvae or pupae. Larvae were sized using the body measurement scale that was developed for the southwestern corn borer (Sloderbeck, 1990). Larvae and pupae number per plant and their locations within the plant, i.e., reproductive or vegetative shoot, were recorded. During May through June each year, the field plot was inspected weekly for adult southern corn stalk borers by walking through the plot and recording the number of adult moths that either took flight from or were seen on the plant materials. Cumulated growing degree days were calculated from 1 January each year using the ‘‘optimum day method’’ (Barger, 1969). Degree days were calculated by averaging the daily maximum and minimum temperatures minus 10uC. For calculation purposes, a temperature of 30uC was used when the daily maximum temperature was greater than 30uC and a temperature of 10uC was used when the daily minimum temperature was less than 10uC. We chose 30uC for an upper threshold temperature based on the research of Cartwright (1934) who reported the shortest developmental times for egg hatch and pupation for southern corn stalk

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borer at that temperature. The lower threshold temperature of 10uC was chosen because this is the typical soil and average air temperature at the time period when the grass is normally burned to remove plant residue. Because a limited number of individuals were collected each year for some life stages, the data for 2003 and 2004 were combined before analysis. The SAS procedure PROC UNIVARIATE (SAS Institute, 1999) was used to generate descriptive statistics for cumulated growing degree days (cGGD) for each life stage and generation, and these statistics were used to describe the life stages of this insect. The 99% quantile of the fitted normal distribution for cGGD was used to describe over-wintering larvae (first through fifth instar), and the 5% quantile of the fitted normal distribution for cGGD was used to describe the first occurrence of pupae from the over-wintering population. The 1% quantile of the fitted normal distribution for cGGD was used to describe the first occurrence of adults from the over-wintering population. Similarly, the 1% quantile of the fitted normal distribution for cGGD was used to describe first occurrences for all life stages of the first and second generation populations. Results and Discussion The life stages of the southern corn stalk borer in eastern gamagrass can be described by three distinct populations in northwestern Oklahoma: the overwintering population (G0), the first generation population (G1), and the second generation population (G2). The G0 population consisted of first through fifth instar larvae, pupae, and adults. Third through fifth instar larvae comprised 83% of the population and traced their origin to the previous G2 population. Over-wintering first and second instar larvae in all probability originated in a prior third generation population. First and second instar larvae comprised 7% of the G0 population, which suggested the beginning of a third generation population the previous year. Data furthermore suggested that only a few of the first or second instar larvae survived the winter. Low numbers of these larvae, a decline in the nutritional quality of the food supply, and/or cannibalism of smaller by larger larvae may explain why these larvae failed to survive the winter. Rarely did we find more than one larva per feeding cavity. These data support the general findings of Cartwright (1934) for corn in South Carolina. Cartwright reported cannibalism of smaller larvae by larger and that a partial third generation was possible in the southern and eastern parts of that state. The nutritional quality of the food supply coupled with cGGD may trigger fourth and fifth instar larvae to pupate. The 99% quantile for fourth and fifth instar larvae was estimated at 456 and 449 cGGD, respectively (Table 1). The 5% quantile for pupae was estimated at 441 cGGD (Table 1). In northwestern Oklahoma, total nonstructural carbohydrates (TNC) of eastern gamagrass shoots peak about the first day of winter at 590 mg of TNC per shoot and decline rapidly to 460 mg per shoot by 31 March (around 211 cGGD) and to a low of 50 mg per shoot by 31 May (around 706 cGGD; Dewald and Sims, 1981). Dietary carbohydrates have been shown to play a significant role in the feeding behavior and growth of the southwestern corn borer (Chippendale and Reddy, 1974). Their data likely applies to the southern corn stalk borer as well. In addition to a decline in food quality, field plots were burned each year about 20 March (at approximately 167 cGGD) to remove plant residue. The charcoaled soil surface and plant crown allowed these

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Table 1. Putative life-stages of the southern corn stalk borer by generations in field grown eastern gamagrass at Woodward, OK. cGGD{ cGGD{ Mean 6 SD

Life-stage

Generation

n

1st Instar 2nd Instar 3rd Instar 4th Instar 5th Instar Pupae

G0 G0 G0 G0 G0 G0

18 74 245 470 434 15

Adult 1st Instar 2nd Instar 3rd Instar 4th Instar 5th Instar Pupae Adult* 1st Instar 2ndInstar 3rd Instar 4th Instar 5th Instar

G0 G1 G1 G1 G1 G1 G1 G1 G2 G2 G2 G2 G2

124 84 131 240 207 137 41

Pupae

G2

3

10 41 58 177 400

2172 10 21 30 12 551

6 6 6 6 6 6

192 173 243 215 219 67

732 6 33 1291 6 154 1405 6 172 1482 6 159 1546 6 122 1622 6 106 1636 6 75 1679 1947 6 119 1987 6 88 2122 6 60 2348 6 89 2524 6 111

Quantile %

Observed{

Estimate{

99 99 99 99 99 5 50 95 1 1 1 1 1 1 1 1 1 1 1 1 1 5 50 95

46 552 456 456 366 457 552 625 654 901 1001 1093 1276 1389 1546

201 339 513 456 449 441 551 662 655 931 1005 1112 1263 1375 1462 1566 1668 1783 1982 2141 2266 2342 2524 2706

1656 1866 2052 2155 2293 2331 2522 2664

2300 6 77

{ Observed, the observed percentage of the observations in each quantile interval; Estimated, the estimated percentage of the population that falls into each quantile interval (estimated from the fitted normal distribution). { Cumulated growing degree days (cGGD) were cumulated from 1 January and were calculated by averaging the daily maximum and minimum temperatures minus 10uC. For calculation purposes, a temperature of 30uC was used when the daily maximum temperature was greater than 30uC. Similarly, a temperature of 10uC was used when the daily minimum temperature was less than 10uC. * Estimate was calculated using the G0 adult population.

exposed surfaces to warm more quickly than surfaces covered with plant residue. Burning was also effective in killing about 15% of the larvae. Pupation was estimated to begin about 333 cGGD (a 1% quantile for pupae). It appeared that pupae remained in an inactive state until about 551 GGD had been accumulated (Table 1). Adult southern corn stalk borers were observed at 654 cGGD, completing the G0 population. Coincidently, TNC levels in eastern gamagrass shoots are at their lowest (Dewald and Sims, 1981) when G0 adult southern corn stalk borers emerge. The first physical signs of the G1 population were egg masses found on the abaxial surfaces of the leaves. Once eggs hatched, the larvae fed in the local area where eggs were laid which created a ‘‘windowpane’’ effect on the leaf. Larvae eventually bored into the base of the culm or into the proaxis, where they continued to feed. Larval feeding caused extensive damage, to the point of culm death. The 1% quantile of fifth instar larvae of the G1 population was estimated at 1375 cGGD (Table 1). Pupation occurred within the feeding cavity and the 1% quantile for pupae was

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estimated at 1462 cGGD. This value was 84 GGD less than what was observed (1546 cGGD, Table 1). Metamorphosis completed when adult southern corn stalk borers emerged from the feeding cavity at about 1566 cGGD. The life cycle of the G1 population of southern corn stalk borers in eastern gamagrass was completed in approximately 911 GGD (1566 cGGD for G1 adults minus 655 cGGD for G0 adults, Table 1). The G2 population began about 1 August (an estimated 1566 cGGD; Table 1) and followed much the same GGD timeline as the G1 population. Assuming it takes 911 cGGD to complete the life cycle of the southern corn stalk borer, the G2 population would complete its life cycle by 22 October (an estimated 2477 cGGD from 1 January). Only three pupae were recovered for the G2 population which made it difficult to give reliable estimates for this generation. In general, pupae were difficult to recover. Because it took approximately 102 GGD for pupation to occur, it was thought that the weekly sampling schedule or, most likely, sampling variation precluded the recovery of pupae in the G1 and G2 populations. In addition, the G2 population life cycle was likely terminated by freezing temperatures. One major difference between the G1 and G2 populations was the duration of the life cycle. The G1 and G2 populations completed their life cycles in approximately 66 and 86 days, respectively. The average time reported for non-hibernating southern corn stalk borers to develop from egg to adult was 50 days with a range of 33 to 76 days for insects reared in captivity on a diet of freshly cut corn stalks or leaves (Cartwright, 1934). The duration of the life cycle for the G1 population fell within the range reported by Cartwright (1934), but the G2 population did not. Diet quality for the G2 population likely explained this difference. Karowe and Martin (1989) found that diets containing 3.4–4.7% nitrogen (20.9–30.5% protein) produced maximum growth rates for fifth instar southern armyworm [Spodoptera eridania (Cramer)] larvae, but growth decreased significantly with higher and lower values of dietary nitrogen. They also reported a larval survival rate of 28% for diets containing 1.8% nitrogen (8.0% protein). They concluded that maximum growth rates and survival occurred when artificial diets contained dietary nitrogen levels that fell within the range found in nature. This also may be the case for southern corn stalk borer, but with slightly different nitrogen thresholds from eastern gamagrass. The nitrogen content of eastern gamagrass forage varies from 2.3–3.1% (14.6–19.6% crude protein) in May to 0.8–1.2% (5.3–7.6% crude protein) in August (Gillen et al., 1999). Plausibly, the greater nitrogen content diet of insects of the G1 population produced a faster growth rate. Another observation worth noting was that larvae occurred 2.5 times more often in reproductive shoots than in vegetative shoots [4.0 6 2.8 (larvae + pupae) in vegetative shoots versus 10.0 6 6.2 in reproductive shoots] which suggested an oviposition preference by adult females for reproductive shoots. This ovipositional preference was influenced by the tendency of reproductive shoots to be the highest points in the canopy when egg lay occurred. A loss of eastern gamagrass seed production over time may be explained by the preference of reproductive culms by southern corn stalk borer females. Eastern gamagrass, recognized as a productive and palatable forage grass species (Magoffin, 1831; Rechenthin, 1951), is an important component of forage and livestock production systems in the central and eastern United States. As the acreage of eastern gamagrass has increased over the past 25 years, the incidences of disease

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and insect pests have become more evident. Our research elucidating the life cycle of one of these major pests, the southern cornstalk borer, is an important contribution in determining methods to manage the pest’s detrimental impact on this forage crop. Acknowledgements We thank Darby Baker, Bill Cooper, Derek Crain, Emalee Friend, Elizabeth Saladin, Kye Schnoebelen, Dana Smith, and Michele Thornton for technical support during this project, and Tom Popham, retired USDA-ARS Statistician, for statistical help. All programs and services of the USDA are offered on a nondiscriminatory basis without regard to race, color, national origin, religion, sex, age, marital status, or handicap. Literature Cited Ainslie, G. G. 1919. The larger corn stalk-borer. USDA Farmer’s Bulletin 1025, Washington, D.C. Barger, G. L. 1969. Total growing degree days. Weekly Weather Crop Bulletin 56:10. Bergquist, R. R. 1981. Transfer from Tripsacum dactyloides to corn of a major gene locus conditioning resistance to Puccinia sorghi. Phytopathology 71:518–520. Cartwright, O. L. 1934. The southern corn stalk borer in South Carolina. South Carolina Agricicultural Experiment Station Bulletin 294, Clemson Agricicultural College, Clemson, SC. Chippendale, G. M., and G. P. V. Reddy. 1974. Dietary carbohydrates: Role in feeding behavior and growth of the southwestern corn borer, Diatraea grandiosella. Journal of Insect Physiology 20:751–759. Dewald, C. L., and B. Kindiger. 1996. Registration of FGT-1 eastern gamagrass germplasm. Crop Science 36:219. Dewald, C. L., and V. H. Louthan. 1979. Sequential development of shoot system components in eastern gamagrass. Journal of Range Management 32:147–151. Dewald, C. L., and P. L. Sims. 1981. Seasonal vegetation establishment and shoot reserves of eastern gamagrass. Journal of Range Management 34:300–304. de Wet, J. M. J. 1979. Tripsacum introgression and agronomic fitness in maize (Zea mays L.), In A. M. van Harten and A. C. Zeven (eds.). Proceedings, Broadening the genetic base of crops, pp. 203–210. Pudoc, Wageningen, The Netherlands. Gillen, R. L., W. A. Berg, C. L. Dewald, and P. L. Sims. 1999. Sequence grazing systems on the southern plains. Journal of Range Management 52:583–589. Heinrichs, E. A., J. E. Foster, and M. E. Rice. 2000. Maize insect pests in North America [Online]. Available at http://ipmworld.umn.edu/chapters/maize.htm (verified 10 April 2008). Howard, L. O. 1891. The larger corn stalk-borer (Diatraea saccharalis Fab.). Insect Life 4:95–103. Karowe, D. N., and M. M. Martin. 1989. The effects of quantity and quality of diet nitrogen on the growth, efficiency of food utilization, nitrogen budget, and metabolic rate of fifth-instar Spodoptera eridania larvae (Lepidoptera: Noctuidae). Journal of Insect Physiology 35:699–708. Krizek, D. T., M. Alma Solis, P. A. Touhey, J. C. Ritchie, and P. D. Millner. 2003. Rediscovery of the southern cornstalk borer: a potentially serious pest of eastern gamagrass and strategies for mitigation. In J. C. Burns (ed.). Proceedings of the Eastern Native Grass Symposium 3rd, pp. 277– 283. Chapel Hill, NC. 1–3 October 2002, Omni Press, Madison, WI. Maas, D. L., and T. L. Springer. 2005. Southern corn stalk borer feeding damage on eastern gamagrass in Oklahoma. Southwestern Entomologist 30:67–69. Magoffin, J. 1831. Gama grass. The American Farmer. Vol. XIII, 143–144. Moellenbeck, D. J., B. D. Barry, and L. L. Darrah. 1995. Tripsacum dactyloides (Gramineae) seedlings for host plant resistance to the western corn rootworm (Coleoptera: Chrysomelidae). Journal of Economic Entomology 88:1801–1803. Phillips, W. J., G. W. Underhill, and F. W. Poos. 1921. The larger stalk borer in Virginia. Virginia Agricultural Experiment Station Technical Bulletin 22. Virginia Polytechnic Institute, Blacksburg, VA.

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Rechenthin, C. A. 1951. Range grasses in the Southwest; eastern gamagrass, Texas cupgrass, Pan American balsamscale and smooth cordgrass. Cattleman 38:110–112. SAS Institute, Inc. 1999. SAS/STATH user’s guide, SAS OnlineDocH, Version 8. Cary, NC. Sloderbeck, P. E. 1990. Identification of European and southwestern corn borers and how to size their larvae, In Southwest Kansas Entomology Update, Vol. 8. No. 6, 2 pp. Kansas Agricultural Experiment Station, Southwest Kansas Research Extension Center, Garden City. Springer, T. L., and C. L. Dewald. 2004. Eastern gamagrass and other Tripsacum species, In L. E. Moser, B. L. Burson, and L. E. Sollenberger (eds.). Warm-season (C4) grasses. Agronomy Monograph number 45, pp. 955–973. ASA-CSSA-SSSA, Madison, WI. Springer, T. L., D. L. Maas, R. L. Gillen, and P. L. Sims. 2003. The maize billbug and Diatraea spp.: Insects affecting the seed production of eastern gamagrass. Proceedings 5th International Herbage Seed Conference, Gatton, Australia, 23–26 November 2003. Springer, T. L., P. L. Sims, and R. L. Gillen. 2004. Estimate of forage yield loss in eastern gamagrass due to shoot boring insects. Proceedings American Forage and Grassland Council, Roanoke, VA. CDROM Vol. 13. 12–16 June 2004.