Terri L. Randolph

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

Abstract 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.

Plant Responses to Seven Russian Wheat Aphid (Hemiptera: Aphididae) Biotypes Found in the United States

ABSTRACT 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.

Cyclical Parthenogenetic Reproduction in the Russian Wheat Aphid (Hemiptera: Aphididae) in the United States: Sexual Reproduction and Its Outcome on Biotypic Diversity

ABSTRACT In 1986, the Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Hemiptera: Aphididae), became an invasive species of United States. Nearly 20 yr later, new biotypes appeared that were capable of overcoming most sources of resistance and became a renewed threat to wheat, Triticum aestivum L., production. Cyclical (CP) and obligate (OP) parthenogenesis enables aphids to both adapt to changing environments and exploit host resources. We documented these forms of reproduction for Russian wheat aphid in wheat and wild grasses in the Central Great Plains and Rocky Mountain regions during falls 2004–2009. Colonies from sample sites also were held under unheated greenhouse conditions and observed for the presence of sexual morphs and eggs through the winter. Russian wheat aphid populations were mainly OP and attempted to overwinter as adults, regardless of region sampled. A few populations contained oviparae but no males (gynocyclic) and were not specific to any particular region. Observation of the Russian wheat aphid colonies under greenhouse conditions failed to produce males or eggs. In spring 2007, CP was confirmed in a small population of Russian wheat aphid that eclosed from eggs (fundatricies) on wild grasses and wheat near Dove Creek, CO, in the Colorado Plateau region where other aphid species undergo CP. Lineages from ninety-three fundatricies were screened against 16 resistant and susceptible cereal entries to determine their biotypic classification. A high degree of biotypic diversity (41.4%) was detected in this population. Although CP was a rare in Russian wheat aphid populations, genetic recombination during the sexual cycle creates new biotypes and can have significant effects on population genetics.

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.

Characterization of Eight Russian Wheat Aphid (Hemiptera: Aphididae) Biotypes Using Two-Category Resistant-Susceptible Plant Responses

ABSTRACT Eight biotypes of the Russian wheat aphid, Diuraphis noxia (Kurdjumov), have been discovered in the United States since 2003. Biotypes are identified by the distinct feeding damage responses they produce on wheat carrying different Russian wheat aphid resistance genes, namely, from Dn1 to Dn9. Each Russian wheat aphid biotype has been named using plant damage criteria and virulence categories that have varied between studies. The study was initiated to compare the plant damage caused by all the eight known Russian wheat aphid biotypes, and analyze the results to determine how Russian wheat aphid virulence should be classified. Each Russian wheat aphid biotype was evaluated on 16 resistant or susceptible cereal genotypes. Plant damage criteria included leaf roll, leaf chlorosis, and plant height. The distribution of chlorosis ratings followed a bimodal pattern indicating two categories of plant responses, resistant or susceptible. Correlations were significant between chlorosis ratings and leaf roll (r2 = 0.72) and between chlorosis ratings and plant height (r2 = 0.48). The response of 16 cereal genotypes to feeding by eight Russian wheat aphid biotypes found RWA1, RWA2, RWA6, and RWA8 to differ in virulence, while Russian wheat aphid biotypes RWA3, RWA4, RWA5, and RWA7 produced similar virulence profiles. These biotypes have accordingly been consolidated to what is hereafter referred to as RWA3/7. Our results indicated that the five main biotypes RWA1, RWA2, RWA3/7, RWA6, and RWA8 can be identified using only four wheat genotypes containing Dn3, Dn4, Dn6, and Dn9.

Reproductive Rates of Russian Wheat Aphid (Hemiptera: Aphididae) Biotypes 1 and 2 on a Susceptible and a Resistant Wheat at Three Temperature Regimes

Abstract 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°C temperature regime than the 13–18°C and 18–24°C temperature regimes. The intrinsic rate of increase was higher for both biotypes at the 18–24°C and 24–29°C temperature regimes than at the 13–18°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°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

Abstract 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.

Change in Biotypic Diversity of Russian Wheat Aphid (Hemiptera: Aphididae) Populations in the United States

ABSTRACT A key component of Russian wheat aphid, Diuraphis noxia (Kurdjumov), management has been through planting resistant wheat cultivars. A new biotype, RWA2, appeared in 2003 which caused widespread damage to wheat cultivars containing the Dn4 gene. Biotypic diversity in Russian wheat aphid populations has not been addressed since 2005 when RWA2 dominated the biotype complex. Our objectives were to determine the biotypic diversity in the Central Great Plains and Colorado Plateau at regional (2010, 2011, 2013) and local (2012) levels and detect the presence of new Russian wheat aphid biotypes. Regional and within-field aphid collections were screened against Russian wheat aphidresistant wheat genotypes containing genes Dn3, Dn4, Dn6, Dn7, Dn9, CI2401; and resistant barley STARS 9301B. In 2010, all aphid collections from Texas were avirulent to the Dn4 resistance gene in wheat. Regional results revealed Dn4 avirulent RWA6 was widespread (55–84%) in populations infesting wheat in both regions. Biotypes RWA1, 2, and 3/7 were equally represented with percentages <20% each while RWA8 was rarely detected. Combining percentages of RWA1, 6, and 8 across regions to estimate avirulence to Dn4 gene revealed high percentages for both 2011 (64–80%) and 2013 (69–90%). In contrast, the biotype structure at the local level differed where biotype percentages varied up to ≥2-fold between fields. No new biotypes were detected; therefore, Dn7, CI2401, and STARS9301B remained resistant to all known Russian wheat aphid biotypes. This study documents a shift to Dn4 avirulent biotypes and serves as a valuable baseline for biotypic diversity in Russian wheat aphid populations prior to the deployment of new Russian wheat aphid-resistant wheat cultivars.

Examining the Competitive Advantage of Diuraphis noxia (Hemiptera: Aphididae) Biotype 2 Over Biotype 1

ABSTRACT 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 of D. 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.

Seasonal Presence of the Russian Wheat Aphid (Hemiptera: Aphididae) on Alternate Hosts in Colorado

Abstract. Russian wheat aphid populations have been monitored for the development of biotypes since the pest first appeared in the United States. Recent studies have confirmed the presence of five unique Russian wheat aphid biotypes in Colorado (Haley et al. 2004, Weiland et al. 2008), two of which were found on noncultivated grass hosts. The objective of this study was to confirm that while the Russian wheat aphid has undergone many changes as a species, the important grass hosts have not changed and are consistent each season. Species of noncultivated grass hosts were inventoried at field sites in four Colorado counties, Baca County, Montezuma County, Washington County, and Weld County, and the presence of Russian wheat aphids on the identified hosts was documented. Field sites were sampled in spring and fall 2005–2006 and the number and species of grass hosts were recorded and compared to look at host consistency across different geographic locations. Twenty-three grass species were identified across all counties. In Baca County, six of 14 grass species hosted Russian wheat aphids. In Montezuma County, Russian wheat aphids were found on five of 13 grass species. In Washington County, Russian wheat aphids were found on six of 18 grass species, and in Weld County, the aphid was found on five of eight grass species. Russian wheat aphids were collected most consistently from crested wheatgrass, Agropyron cristatum (L.) Gaertn., downy brome, Bromus tectorum L., Canada wildrye, Elymus canadensis L., and intermediate wheatgrass, Thinopyrum intermedium (Host) Barkw. & D.W.