Unexpectedly High Levels of Parasitism of Wheat Stem Sawfly Larvae in Postcutting Diapause Chambers Author(s) :Tatyana A. Rand, Debra K. Waters, Thomas G. Shanower Source: The Canadian Entomologist, 143(5):455-459. 2011. Published By: Entomological Society of Canada URL: http://www.bioone.org/doi/full/10.4039/n11-023

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. 455 Unexpectedly high levels of parasitism of wheat stem sawfly larvae in postcutting diapause chambers

Tatyana A. Rand, Debra K. Waters, Thomas G. Shanower

Abstract*We examined rates of late-season parasitism of larvae of the wheat stem sawfly, Cephus cinctus Norton (Hymenoptera: Cephidae), by native species of Bracon F. (Hymenop- tera: Braconidae) over 8 years in Montana and North Dakota, United States of America. We found that rates of parasitism of larvae in diapause chambers reached a maximum of 46%, exceeding the previously reported maximum of 2.5% in 75% of sites and years examined. In contrast to previous work, our results demonstrate that C. cinctus larvae are suitable hosts for braconid parasitoids, even after the formation of diapause chambers, and suggest that parasitism rates may be underestimated if stems are sampled prior to harvest.

Re´sume´*Nous examinons les taux de parasitisme en fin de saison chez les larves du ce`phe du ble´, Cephus cinctus Norton (Hymnenoptera: Cephidae), par les espe`ces indige`nes de Bracon F. (Hymenoptera: Braconidae) sur une pe´riode de 8 ans dans le Montana et le Dakota du Nord, E´ tats-Unis. Les taux de parasitisme des larves en diapause dans leur logette atteignent un maximum de 46 %, ce qui de´passe le maximum de 2,5 % enregistre´ ante´rieurement dans 75 % des sites et anne´es examine´s. Contrairement aux travaux pre´ce´dents, nos re´sultats de´montrent que les larves de C. cinctus sont des hoˆtes approprie´s pour les parasito¨ıdes braconide´s, meˆme apre`s la formation des logettes de diapause; il se peut que les taux de parasitisme aient e´te´ sous- estime´s par le pre´le`vement des tiges avant la pe´riode des re´coltes.

[Traduit par la Re´daction] Introduction pressure on larvae of C. cinctus in wheat in some regions (Morrill 1997; Runyon et al. The wheat stem sawfly, Cephus cinctus Nor- 2001). Females of both Bracon species locate, ton (Hymenoptera: Cephidae), is the most paralyze, and then lay eggs on larvae of important pest of wheat, Triticum aestivum L. (Poaceae), in the northern Great Plains of C. cinctus within stems; the braconid larvae the United States of America (Morrill and develop as ectoparasitoids (Nelson and Kushnak 1999; Shanower and Waters 2006). Farstad 1953; Somsen and Luginbill 1956; Yield losses occur in part as a result of lodging Holmes et al. 1963). The location of a para- resulting from the girdling of stem bases by the sitoid reflects the position of a larvawhen it was stem-mining larvae. Larvae subsequently form initially parasitized. First-generation parasi- diapause chambers in the resultant stem stubs, toids develop rapidly and enter a short pupal in which they overwinter. Larvae of two native stage, adults emerge, and a complete or braconid wasps, Bracon cephi (Gahan) and partial second generation follows (Nelson Bracon lissogaster Muesebeck (Hymenoptera: and Farstad 1953; Somsen and Luginbill Braconidae), exert significant parasitism 1956). Second-generation adult parasitoids

Received 15 February 2011. Accepted 28 April 2011. T.A. Rand,1 D.K. Waters, United States Department of Agriculture, Agricultural Research Service, Northern Plains Agricultural Research Laboratory, Sidney, MT 59270, United States of America T.G. Shanower, United States Department of Agriculture, Agricultural Research Service, Center for Grain and Animal Health Research, Manhattan, KS 66502, United States of America 1Corresponding author (e-mail: [email protected]). doi: 10.4039/n11-023

Can. Entomol. 143: 455459 (2011) # 2011 Entomological Society of Canada 456 Can. Entomol. Vol. 143, 2011 are present from the middle of August through to break diapause. Samples were then removed late September (Nelson and Farstad 1953), from cold treatment and 50100 stubs were which is mostly after wheat harvest in the placed upright in 454 g plastic containers, northern Great Plains. covering the base of the stubs with a small The lack of late-season hosts on which amount of potting soil. Containers with stubs second-generation Bracon species can com- were placed inside sealable perforated 3.8 L plete development, and thereby increase in plastic bags (two containers per bag). These numbers, has been considered a major factor were maintained in the laboratory at 2125 8C limiting their success in controlling C. cinctus under fluorescent lighting with a 16L:8D (Holmes et al. 1963; Morrill et al. 1994). cycle, keeping the soil moist by spraying daily Holmes et al. (1963) observed that B. cephi with distilled water. rarely attacks C. cinctus successfully once it Stubs were monitored daily and emerging has formed overwintering chambers (this gen- C. cinctus and parasitoids were quantified and erally occurs when the moisture levels in the removed using an aspirator until emergence host plant drop below 50%, just prior to wheat ceased. Proportion parasitism was calculated harvest). Maximum rates of parasitism of as the number of Bracon spp. parasitoids C. cinctus by B. cephi in at least 600 stubs divided by the total number of emergent collected annually between 1953 and 1960 Bracon spp. and C. cinctus individuals com- near Lethbridge, Alberta, Canada, was 2.5% bined. We pooled parasitoid numbers because (Holmes et al. 1963). Here we report on results the two Bracon species are difficult to distin- of a study designed to examine the generality guish morphologically (Runyon et al. 2001). of these findings by quantifying rates of Bracon cephi has previously been found to be parasitism of C. cinctus larvae in diapause the dominant parasitoid in eastern Montana chambers in wheat stubble after harvest (Meers 2005) and thus likely dominated our during an 8-year period in Montana and samples. North Dakota.

Preharvest stem collection and dissection Materials and methods Sites used in 20012004 were long-term research sites for which we also collected Postharvest stub collection and processing data on rates of C. cinctus stem infestation Stems that had been cut by C. cinctus to and parasitism. Between 87 and 151 stems form diapause chambers (hereinafter referred were collected just prior to harvest at each to as stubs) were collected after wheat harvest site in each year (Table 1), brought back to in Montana (Richland, Daniels, and Valley the laboratory, and dissected to assess rates of counties) and North Dakota (Golden Valley C. cinctus infestation and parasitism. Stems County), United States of America (Table 1) that contained any evidence of C. cinctus in the fall or early in the spring before the soil (eggs, larvae, or characteristic feeding damage warmed above 12 8C. Collections were made and frass) were considered infested. The pre- in one to three wheat fields per year between sence of Bracon spp. within stems was also 2001 and 2009, except in 2008. noted. Evidence of parasitoids included larvae In each sampling site-year, wheat stubble of Bracon spp. feeding externally on C. cinctus, was excavated and brought to the laboratory, cocoons present within the stems, or the where stubs were separated from uncut stems, presence of characteristic exit holes. Parasit- and carefully cleaned of excess soil and roots. ism was calculated as the number of stems More than 100 stubs were collected in each containing evidence of parasitism divided by site-year (Table 1). Stubs were placed into the number of stems infested by C. cinctus. sealable perforated 3.8 L plastic bags, lightly We fit general linear models using the sprayed with distilled water, and placed in cold REML (REstricted Maximum Likelihood) storage at 48 8C for a minimum of 120 days method in JMP version 8.0.1 (SAS Institute

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Table 1. Location, sample sizes, and collection dates for each site and year of the study of parasitism of Cephus cinctus in North Dakota and Montana.

Location* Latitude Longitude No. of stubs No. of stems Collection Year Site (N) (W) collected Collection dates collected date 2001 1 48.6406 105.2354 3164 10 Sept. 1 Nov. 87 28 Aug. 2 48.8384 106.3281 268 26 Oct. 151 21 Aug. 2002 1 48.6406 105.2354 153 12 Mar. 99 27 Aug. 2 48.8384 106.3281 883 512 Mar. 111 27 Aug. 2003 1 48.6406 105.2354 2504 12 Sept. 23 Oct. 104 11 Aug. 2 48.8384 106.3281 1166 3 Apr. 102 31 July 2004 1 48.6406 105.2354 3645 2229 Oct. 129 5 Aug. 2005 1 48.6406 105.2354 3598 1219 Oct. NA NA 3 48.6571 105.2951 3738 37Nov. NA NA 2006 3 48.6571 105.2951 400 1819 Oct. NA NA 4 46.8614 103.9596 1775 1827 Oct. NA NA 5 46.9667 104.0074 815 2527 Oct. NA NA 2007 4 46.8614 103.9596 333 1 Nov. NA NA 5 46.9667 104.0074 188 1 Nov. NA NA 2009 6 47.7323 104.4867 2635 522 Mar. NA NA 7 47.7032 104.4518 3011 24 Apr. NA NA Note: Stubs were collected after harvest in fall-winter, while stems were collected prior to harvest (summer) in each year. *Coordinates are given in decimal degrees (NAD 83).

Inc. 19892011) to assess the influence of Fig. 1. Percent parasitism of Cephus cinctus larvae sample size (number of stubs collected) on in diapause chambers (stubs) in wheat at seven sites proportion parasitism in stubs. Similar models in North Dakota and Montana from 2001 to 2009. were run to examine the influence of the proportion of stems infested by C. cinctus on 50 Site 1 the proportion of parasitized larvae in stems Site 2 Site 3 and stubs and the relationship between stem 40 Site 4 Site 5 parasitism and stub parasitism. Proportion- in stubs Site 6 Site 7 parasitism data were arcsine square-root- 30 transformed for all models.

20

Results 10

Percentage parasitism We collected over 28000 stubs; numbers per 0.0 site-year varied considerably (Table 1). Rates 2001 2002 2003 2004 2005 2006 2007 2009 of parasitism were not significantly related to Sampling year sample size (F1,14 2.36, P 0.1470) and 2 varied between sites and across years (Fig. 1; that in stubs (Figure 2, Radj. 0.58, F1,6 range 0.5%46%). Rates were much higher 10.64, P 0.0172; y 0.0378 0.6654x). than expected based on previous work, exceed- Although parasitism of larvae in stems was ing the previous maximum observed rate of positively related to levels of C. cinctus infesta- 2 2.5% (Holmes et al. 1963) in 12 of 16 site-years. tion (Radj. 0.57, F1,6 10.54, P 0.0175; Parasitism of C. cinctus larvae in stem samples y 0.1116 0.8289x), this was not the case was similarly variable (range 1.5%75.5%) for parasitism of larvae in stubs (F1,6 1.15, and was significantly positively related to P 0.3248).

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Fig. 2. Relationship of percent parasitism of Regional differences are unlikely to explain C. cinctus larvae in wheat stems and diapause the differences between our results and those chambers (stubs) at long-term study sites in North previously reported by Holmes et al. (1963), Dakota and Montana from 2001 to 2004. given that Ca´rcamo et al. (2011) found similarly high average rates of parasitism 50 (10%20%) near Lethbridge, Alberta. Instead, we suspect that the widespread adoption of

40 no- or minimum-tillage practices across the Northern Plains reduces the negative effects of in stubs tillage on parasitoids (Runyon et al. 2002; 30 Weaver et al. 2004). These practices leave stubs on the soil surface, where they are more 20 vulnerable to parasitoid attack than if they have been tilled under. 10 Our results have two important implications.

Percentage parasitism First, given that C. cinctus larvae are clearly

0 viable hosts for the native braconids B. cephi 020406080and B. lissogaster, even after the formation of Percentage parasitism in stems diapause chambers, total parasitism rates may be significantly underestimated if stems are Discussion sampled prior to harvest. Thus, the potential cross-generational benefits of the braconids Holmes et al. (1963) found that C. cinctus may have been generally underappreciated. larvae generally escape parasitism once they Second, the argument that a lack of late-season have girdled stems to form their overwintering hosts is a major factor limiting the success of the chambers, and observed a maximum parasit- braconids clearly warrants more careful scru- ism rate of 2.5%. Morrill et al. (1994) also tiny, given evidence that C. cinctus larvae in noted low parasitism in stubs but did not diapause chambers in wheat are suitable hosts. present data. Holmes et al. (1963) further Further research along these lines will be suggested that suitable hosts are often absent critical to understanding the population dy- late in the season, when second-generation namics of B. cephi and B. lissogaster and adult parasitoids are active. developing management strategies to conserve Our results suggest that the generality of and augment these potentially important bio- those conclusions should be critically reeval- logical agents for controlling C. cinctus. uated. We found that parasitism of C. cinctus larvae in postcutting diapause chambers can be substantial, reaching a maximum of 46% Acknowledgements (mean 14.8%), which contrasts dramatically Kevin Delaney, He´ctor Ca´rcamo, Robb with the maximum rate of 2.5% previously Bennett, and an anonymous reviewer provided reported. Furthermore, parasitism exceeded helpful comments on the manuscript. We these rates in 75% of the site-years examined in our study. Not surprisingly, we also found additionally thank the growers who allowed that parasitism rates in diapause chambers us to collect stubs from their fields. were positively related to those in wheat stems collected prior to harvest, exceeding them in References three cases. Rearing hosts through until parasitoid emergence tends to underestimate Ca´rcamo, H.A., Herle, C., Beres, S.B.L., McLean, H., and McGinn, S. 2011. Solid-stemmed wheat parasitism relative to dissection (Day 1994) does not affect overwintering mortality of and therefore our estimates of parasitism in Cephus cinctus. Journal of Insect Science. In stubs are likely conservative. press.

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Day, W.H. 1994. Estimating mortality caused by stem sawfly, Cephus cinctus Nort. (Hymenop- parasites and diseases of insects * comparisons tera: Cephidae), in Western Canada. The Cana- of the dissection and rearing methods. Environ- dian Entomologist, 85: 101107. doi: 10.4039/ mental Entomology, 23: 543550. Ent85103-3. Holmes, N.D., Nelson, W.A., Peterson, L.K., and Runyon, J.B., Hurley, R.L., Morrill, W.L., and Farstad, C.W. 1963. Causes of variations in Weaver, D.K. 2001. Distinguishing adults of effectiveness of Bracon cephi (Gahan) (Hyme- Bracon cephi and Bracon lissogaster (Hymenop- noptera: Braconidae) as a parasite of the wheat tera: Braconidae), parasitoids of the wheat stem stem sawfly. The Canadian Entomologist, 95: sawfly (Hymenoptera: Cephidae). The Canadian 113126. doi: 10.4039/Ent95113-2. Entomologist, 133: 215217. doi: 10.4039/ Meers, S.B. 2005. Impact of harvest operation on Ent133215-2. parasitism of the wheat stem sawfly, Cephus Runyon, J.B., Morrill, W.L., Weaver, D.K., and cinctus Norton (Hymenoptera: Cephidae). M.S. Miller, P.R. 2002. Parasitism of the wheat stem thesis, Montana State University, Bozeman, sawfly (Hymenoptera: Cephidae) by Bracon Montana. cephi and B. lissogaster (Hymenoptera: Braconi- Morrill, W.L. 1997. The wheat stem sawfly, Cephus dae) in wheat fields bordering tilled and untilled cinctus, Norton (Hymenoptera:Cephidae), and fallow in Montana. Journal of Economic En- associated parasitoids in the northern Great tomology, 95: 11301134. Plains of North America. Trends in Entomol- SAS Institute Inc. 19892011. JMP version 8.0.1 ogy, 1: 171174. [computer program]. SAS Institute Inc., Cary, Morrill, W.L., and Kushnak, G.D. 1999. Planting North Carolina. date influences on the wheat stem sawfly (Hy- Shanower, T.G., and Waters, D.K. 2006. A survey menoptera: Cephidae) in spring wheat. Journal of five stem-feeding insect pests of wheat in the of Agricultural and Urban Entomology, 16: northern Great Plains. Journal of Entomological 123128. Science, 41:4048. Morrill, W.L., Kushnak, G.D., Bruckner, P.L., and Somsen, H.W., and Luginbill, P. 1956. Bracon Gabor, J.W. 1994. Wheat stem sawfly (Hyme- lissogaster Mues.: a parasite of the wheat stem noptera, Cephidae) damage, rates of parasitism, sawfly. United States Department of Agriculture and overwinter survival in resistant wheat lines. Technical Bulletin No. 1153. Journal of Economic Entomology, 87: 1373 Weaver, D.K., Sing, S.E., Runyon, J.B., and Morrill, 1376. W.L. 2004. Potential impact of cultural practices Nelson, W.A., and Farstad, C.W. 1953. Biology of on wheat stem sawfly (Hymenoptera: Cephidae) Bracon cephi (Gahan) (Hymenoptera: Braconi- and associated parasitoids. Journal of Agricul- dae), an important native parasite of the wheat tural and Urban Entomology, 21: 271287.

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