Phylogeography of the Wheat Stem Sawfly, Cephus cinctus Norton (Hymenoptera: Cephidae): Implications for Pest Management.

The wheat stem sawfly, Cephus cinctus Norton (Hymenoptera: Cephidae), is a key pest of wheat in the northern Great Plains of North America, and damage resulting from this species has recently expanded southward. Current pest management practices are inadequate and uncertainty regarding geographic origin, as well as limited data on population structure and dynamics across North America impede progress towards more informed management. We examined the genetic divergence between samples collected in North America and northeastern Asia, the assumed native range of C. cinctus using two mitochondrial regions (COI and 16S). Subsequently, we characterized the structure of genetic diversity in the main wheat producing areas in North America using a combination of mtDNA marker and microsatellites in samples collected both in wheat fields and in grasses in wildlands. The strong genetic divergence observed between North American samples and Asian congeners, in particular the synonimized C. hyalinatus, did not support the hypothesis of a recent American colonization by C. cinctus. Furthermore, the relatively high genetic diversity both with mtDNA and microsatellite markers offered additional evidence in favor of the native American origin of this pest. The genetic diversity of North American populations is structured into three genetic clusters and these are highly correlated with geography. Regarding the recent southern outbreaks in North America, the results tend to exclude the hypothesis of recent movement of damaging wheat stem sawfly populations from the northern area. The shift in host plant use by local populations appears to be the most likely scenario. Finally, the significance of these findings is discussed in the context of pest management.

Examining the competitive advantage of Diuraphis noxia (Hemiptera: Aphididae) biotype 2 over biotype 1.

The Russian wheat aphid, Diuraphis noxia (Kurdjumov) is a serious pest of small grains, such as wheat and barley. High population growth rates and a broad gramineae host range have allowed this aphid to successfully establish and become pestiferous across much of North America since its invasion in the mid-1980s. Resistant wheat cultivars were developed and provided control ofD. noxia until 2003, when a new biotype (designated RWA2, as contrasted with the original biotype's designation, RWA1) emerged and rapidly spread through dryland winter wheat-growing regions. RWA2 displaced RWA1 more quickly than expected, based on RWA2's advantage in RWA1-resistant wheat cultivars. Previous research suggested that RWA2 may out-compete RWA1 in cooler temperatures. Thus, we sought to determine if RWA2 had a competitive advantage over RWA1 during the overwintering period. We placed a known distribution of RWA1 and RWA2 aphids in the field for the winter at three sites across a latitudinal gradient (from northern Colorado to Texas) to test for a competitive advantage between these biotypes. We found overwhelming support for an overwintering competitive advantage by RWA2 over RWA1, with evidence suggesting a > 10-fold advantage even at our Texas site (i.e., the site with the mildest winter). This substantial overwintering advantage helps explain the quick dispersion and displacement of RWA1 by RWA2.

Plant responses to seven Russian wheat aphid (Hemiptera: Aphididae) biotypes found in the United States.

The Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Hemiptera: Aphididae), is a serious wheat, Triticum aestivum L., and barley, Hordeum vulgare L., pest throughout the small grain-producing areas in the western United States. The virulency and classification of recently described Russian wheat aphid biotypes 1-7 (RWA1-7) were clarified using 24 plant differentials. These seven biotypes had been described previously using various methods and test environments; therefore, the purpose of this study was to test them all under uniform environmental conditions. RWA1 was the least virulent of the biotypes tested, with susceptible ratings observed in five plant differentials and intermediate ratings observed in four plant differentials. RWA4, RWA5, RWA6, and RWA7 had intermediate virulence. RWA4, RWA5, and RWA7 share similar responses, with susceptible responses in six plant differentials and intermediate responses in five plant differentials. Small differences within a few plant differentials separate RWA4, RWA5, and RWA7. RWA6 has susceptible responses with only four plant differentials, but 10 plant differentials had intermediate responses. RWA3 was highly virulent, with susceptible responses in 10 plant differentials and intermediate responses in five plant differentials. RWA2 was the most virulent strain tested with susceptible responses to 12 plant differentials and intermediate responses to five plant differentials. This study has demonstrated that RWA1-7 have different combinations of virulence to the plant differentials tested, thereby confirming previous Russian wheat aphid biotype designations.

Reproductive rates of Russian wheat aphid (Hemiptera: Aphididae) biotypes 1 and 2 on a susceptible and a resistant wheat at three temperature regimes.

The reproductive rates of Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Hemiptera: Aphididae), Biotype 1 (RWA 1) and Biotype 2 (RWA 2) were compared in the laboratory at three temperature regimes on a Russian wheat aphid resistant cultivar ('Prairie Red') and a susceptible cultivar ('TAM 107'). The objective of this study was to expose RWA 1 and RWA 2 to three temperature regimes and two levels of resistance to find whether there were reproductive differences that may occur within each biotype as well as differences in reproduction between biotypes. In addition, temperature effects of the Dn4 gene on biotype reproduction were noted. Differences in reproductive rates between the two biotypes seem to be driven by temperature. For both biotypes, longevity and reproductive rate parameters, except for intrinsic rate of increase, were lower at the 24-29 degree C temperature regime than the 13-18 degree C and 18-24 degree C temperature regimes. The intrinsic rate of increase was higher for both biotypes at the 18-24 degree C and 24-29 degree C temperature regimes than at the 13-18 degree C temperature regime. Reproductive rates between biotypes were similar at the two higher temperature regimes, but the fecundity for RWA 1 was less than RWA 2 at the 13-18 degree C temperature. The change in fecundity rates between RWA 1 and RWA 2 at lower temperatures could have ecological and geographical implications for RWA 2.

Reproduction and development of Russian wheat aphid biotype 2 on crested wheatgrass, intermediate wheatgrass, and susceptible and resistant wheat.

The Russian wheat aphid, Diuraphis noxia (Kurdjumov), is an economically important pest of small grains. Since its introduction into North America in 2003, Russian wheat aphid Biotype 2 has been found to be virulent to all commercially available winter wheat, Triticum aestivum L., cultivars. Our goal was to examine differences in Russian wheat aphid reproduction and development on a variety of plant hosts to gain information about 1) potential alternate host refuges, 2) selective host pressures on Russian wheat aphid genetic variation, and 3) general population dynamics of Russian wheat aphid Biotype 2. We studied host quality of two wheatgrasses (crested wheatgrass, Agropyron cristatum [L.] Gaertn., and intermediate wheatgrass, Agropyron intermedium [Host] Beauvoir) and two types of winter wheat (T. aestivum, one Biotype 2 susceptible wheat, 'Custer' and one biotype 2 resistant wheat, STARS02RWA2414-11). The susceptible wheat had the highest intrinsic rate of increase, greatest longevity and greatest fecundity of the four host studied. Crested wheatgrass and the resistant wheat showed similar growth rates. Intermediate wheatgrass had the lowest intrinsic rate of increase and lowest fecundity of all tested hosts.

Biotypic diversity in Colorado Russian wheat aphid (Hemiptera: Aphididae) populations.

The biotypic diversity of the Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Hemiptera: Aphididae), was assessed in five isolates collected in Colorado. Three isolates, RWA 1, RWA 2, and an isolate from Montezuma County, CO, designated RWA 6, were originally collected from cultivated wheat, Triticum aestivum L., and obtained from established colonies at Colorado State University. The fourth isolate, designated RWA 7, was collected from Canada wildrye, Elymus canadensis L., in Baca County, CO. The fifth isolate, designated RWA 8, was collected from crested wheatgrass, Agropyron cristatum (L.) Gaertn., in Montezuma County, CO. The four isolates were characterized in a standard seedling assay, by using 24 plant differentials, 22 wheat lines and two barley, Hordeum vulgare L., lines. RWA 1 was the least virulent of the isolates, killing only the four susceptible entries. RWA 8 also killed only the four susceptible entries, but it expressed intermediate virulence on seven wheat lines. RWA 6, killing nine entries, and RWA 7, killing 11 entries, both expressed an intermediate level of virulence overall, but differed in their level of virulence to 'CO03797' (Dn1), 'Yumar' (Dn4), and 'CO960293-2'. RWA 2 was the most virulent isolate, killing 14 entries, including Dn4- and Dny-containing wheat. Four wheat lines, '94M370' (Dn7), 'STARS 02RWA2414-11', CO03797, and 'CI2401', were resistant to the five isolates. The results of this screening confirm the presence of five unique Russian wheat aphid biotypes in Colorado.

Comparison of Dn4- and Dn7-carrying spring wheat genotypes artificially infested with Russian wheat aphid (Homoptera: Aphididae) biotype 1.

Genetic resistance is a useful control strategy for managing Russian wheat aphid, Diuraphis noxia (Mordvilko), in wheat, Triticum aestivum L. In 2003, a Russian wheat aphid population (denoted as biotype 2) identified in Colorado was virulent to genotypes carrying the Dn4 Russian wheat aphid resistance gene, necessitating the rapid identification and deployment of new sources of resistance. Although the Dn7 gene had shown excellent resistance to Russian wheat aphid biotypes 1 and 2 in evaluations in the greenhouse, no information is available on the amount of protection provided by Dn7 under field conditions. The objective of this study was to compare the reaction of Dn4- and Dn7-carrying spring wheat genotypes under artificial infestation by Russian wheat aphid biotype 1 in the field. Irrigated field experiments were conducted in 2003 and 2004 in a split-split plot arrangement with six replications. The whole plot treatment was infestation level (control, 1x, and 10x Russian wheat aphids), and the subplot treatment was resistance source (Dn4- and Dn7-carrying genotypes). The sub-subplot treatment consisted of side-by-side planting of resistant and susceptible genotypes. The Dn4 subplot was significantly more damaged than the Dn7 subplot in 2003, but not in 2004. Interaction effects observed in 2004 suggested an advantage of Dn7 relative to Dn4 in terms of reduced Russian wheat aphid abundance and plant damage. Deployment of the Dn7 Russian wheat aphid resistance gene should provide protection in the field comparable with that provided by the Dn4 resistance gene for management of Russian wheat aphid biotype 1.

Influence of three resistance sources in winter wheat derived from TAM 107 on yield response to Russian wheat aphid.

A study to determine yield response to the Russian wheat aphid, Diuraphis noxia (Mordvilko), was conducted during the 1997-1998 and 1998-1999 growing seasons at three eastern Colorado locations, Akron, Fort Collins, and Lamar, with three wheat lines containing either Russian wheat aphid-resistant Dn4 gene, Dn6 gene, or resistance derived from PI 222668, and TAM 107 as the susceptible control. Russian wheat aphids per tiller were greater on TAM 107 than the resistant wheat lines at the 10x infestation level at Fort Collins and Akron in 1999. Yield, seed weight, and number of seeds per spike for each wheat line were somewhat affected by Russian wheat aphid per tiller mainly at Fort Collins. The infested resistant wheat lines harbored fewer Russian wheat aphids and yielded more than the infested susceptible wheat lines. Wheat lines containing the Dn4, Dn6, and PI 222668 genes contain different levels of antibiosis or antixenosis and tolerance. Although differences existed among sites and resistance, there is a benefit to planting resistant wheat when there is a potential for Russian wheat aphid infestations.

Yield response and categories of resistance to Russian wheat aphid in four Dn4 hard red winter wheat cultivars.

A field experiment was conducted to determine whether resistance to Russian wheat aphid, Diuraphis noxia (Mordvilko), conferred by the Dn4 gene is affected by genetic background. This was done by comparing the yield responses to Russian wheat aphid-resistant wheat containing Dn4, derived through the backcross method, to those of the corresponding recurrent parents. Infested resistant cultivars had fewer Russian wheat aphids per tiller than infested susceptible cultivars at the Lamar and Fort Collins, CO sites but not at the Akron, CO site. At the Lamar site, resistant cultivars yielded more than the susceptible cultivars. 'Prairie Red' and 'Yumar' were more resistant than 'Prowers', especially at the higher infestation level. Resistance in these cultivars was categorized in a laboratory experiment to confirm this differential expression of resistance. Resistance in Prairie Red, 'Halt', 'Prowers 99', and Yumar was categorized at three plant growth stages. Antibiosis was expressed as reductions in maximum number of nymphs produced per 24 h and intrinsic rate of increase. The maximum number of nymphs produced per 24 h was reduced in Halt and 'Lamar'. Averaged over cultivars, the intrinsic rate of increase was less at jointing than at the seedling or tillering growth stages. Tolerance was expressed in the resistant cultivars as reduced chlorosis and leaf rolling. Growth reductions in infested Prowers 99 plants was less than the other cultivars. This study confirms that some cultivars containing Dn4 may express antibiosis and tolerance, whereas others may not show the same categories. Thus, expression is affected by genetic background.

Categories of resistance at four growth stages in three wheats resistant to the Russian wheat aphid (Homoptera: Aphididae).

Laboratory experiments were conducted to determine categories of resistance to Russian wheat aphid, Diuraphis noxia (Mordvilko), in three wheats, Triticum aestivum L, (PI 372129, PI 243781, and PI 222668) at Zadoks growth stages 10, 20, 30, and 40. 'TAM 107' was used as the susceptible standard. Antixenosis was observed in PI 222668 and PI 372129. Antibiosis was expressed as reduced nymphipositional period, daily nymph production, and fecundity at the jointing (Zadoks 30) and boot (Zadoks 40) stages in PI 243781 and at tillering (Zadoks 20) in TAM 107. Antibiosis, expressed as reduced intrinsic rate of increase, was observed in PI 222668 at tillering (Zadoks 20). Tolerance to chlorosis and leaf rolling was expressed in the three resistant wheats at all growth stages tested. Tiller production, floret formation, spike length and wet weight were affected by Russian wheat aphid feeding after Zadoks 10. Reduction in spike length did not occur in PI 372129 and PI 243781.

Categories of resistance at different growth stages in halt, a winter wheat resistant to the Russian wheat aphid (Homoptera: Aphididae).

This study was designed to categorize the resistance to the Russian wheat aphid, Diuraphis noxia (Mordvilko), resistant hard red winter wheat, Halt, as compared with susceptible wheat, TAM 107, at four different growth stages. Antixenosis was expressed in Halt at growth stage Zadoks 30. Antibiosis in Halt affected fecundity, number of aphids produced per reproductive day, maximum number of nymphs produced in one day, and intrinsic rate of increase. Fecundity was lower on Halt than TAM 107, and more nymphs were produced on both varieties at growth stage 20 than 10 and 40. Fewer nymphs were produced per reproductive day and on maximum production days by aphids reared on Halt than by those reared on TAM 107. The intrinsic rate of increase of Russian wheat aphids reared on Halt was lower than aphids reared on TAM 107. Differences in plant height and plant dry weight did not occur. Chlorosis ratings showed greater damage at the earlier stages in Halt and TAM 107 and significantly more damage in TAM 107 than Halt at growth stages 10, 20, and 30. Leaf rolling occurred on infested plants of TAM 107 at growth stages 10, 20, and 30, but not growth stage 40. Halt plants did not exhibit leaf rolling. The presence of a significant level of tolerance could make Halt compatible with other integrated pest management programs. However, care should be taken with cultivars containing evidence of antixenosis or antibiosis that could cause selective pressure on the Russian wheat aphid, potentially causing biotypes to be produced.

Plant damage and yield response to the Russian wheat aphid (Homoptera: Aphididae) on susceptible and resistant winter wheats in Colorado.

Plant damage and yield response to the Russian wheat aphid, Diuraphis noxia (Mordvilko), were evaluated on a susceptible (TAM 107) and a resistant (RWA E1) winter wheat, Triticum aestivum L., in three Colorado locations in the 1993 and 1994 crop years. Russian wheat aphid was more abundant on TAM 107 than on RWA E1. Russian wheat aphid days per tiller were greater at the higher infestation levels. Yield losses as a result of Russian wheat aphid infestation occurred most of the time with TAM 107 but rarely with RWA E1. Seed densities were reduced at higher infestation levels in TAM 107 at two locations. Russian wheat aphids per tiller had a negative relationship to yield in TAM 107 but not in RWA E1. In TAM 107 yield decreased as aphid densities increased, but yield remained constant regardless of initial aphid abundance on RWA E1 in all environments. Seed densities were reduced at higher infestation levels in TAM 107 at two locations. The resistance conferred by the Dn4 gene seems to be an effective management approach across a range of field conditions.