Comparison of plant reaction of the five
Russian wheat aphid (RWA) is an international pest on wheat and occurs in most countries where large scale wheat cultivation is practiced. Consequently, considerable efforts have been made to manage RWA globally. The two management options used currently are chemical control and breeding for deployment of resistant wheat cultivars. There are however drawbacks to both of these management practices. Chemical control has a negative impact on the environment, especially other insect groups such as predators, pollinators and decomposers. With widespread and continuous use of the same active ingredients, there is the possibility that RWA can build up resistance against these specific active ingredients. The drawback with resistance breeding is that certain RWA populations can overcome the resistance in the wheat, resulting in new biotypes virulent to the resistant wheat cultivars.
- Russian wheat aphid
- Diuraphis noxia
- Triticum aestivum
- insecticide resistance
Establishment success and rate of spread will determine the invasive ability of a specific organism . The success of an invasive species will further be determined by both abiotic and biotic factors that will influence the adaptation and spread within the geographic range of establishment . Liu
RWA-resistant cultivars were released and deployed in South Africa during 1992, and more than 70% of the wheat production area in South Africa was planted with Russian wheat aphid-resistant cultivars . The durability of resistant cultivars was, however, challenged by the occurrence of RWA biotypes, first in Colorado in 2003 , and in South Africa in 2006 . Russian wheat aphid biotypic variation was also found in Hungary  and Chile . Since 2006, five distinct RWA biotypes have been recorded in the wheat production areas of the Eastern Free state (summer rainfall area), South Africa, RWASA2 in 2006; RWASA3 in 2009; RWASA4 in 2011 and most recently RWASA5 in 2018.
The second management option, chemical control, is also practiced in South Africa, mainly in the Western Cape (winter rainfall area) and on irrigation wheat in central and western Free State and Northern Cape. Chemical control has long term, negative impacts on the environment, especially other insect groups such as predators, pollinators, and decomposers. Hill, et al.  demonstrated that broad spectrum pesticide application in grain crops can lead to secondary outbreaks of pests due to alteration of natural enemy communities. The active ingredients registered for RWA control on wheat in South Africa are limited and include acetamiprid, chlorpyrifos, chlorpyrifos + cypermethrin, demeton-S-methyl, dimethoate, imidacloprid, parathion, prothiofos and thiamethoxam. With widespread and continuous use of these active ingredients, there is the possibility that RWA can build up resistance against these specific active ingredients. About 20 species in the Aphididae have evolved resistance to insecticides  and can be associated with detectable changes in reproductive rates . Brewer and Kaltenbach  demonstrated that there is detectable variation in RWA insecticide susceptibility and reproductive rates after exposure to chlorpyrifos. Chlorpyrifos selection seen in wheat production may result in large scale changes in susceptibility and control failures. Russian wheat aphid variation in virulence to small grains occurs [24, 25] as well as variation in fecundity [26, 27]. There is a possibility that RWA can also evolve virulence to active ingredients in chemicals. In their recommendations for managing RWA expansion into all major grain regions of Australia Ward et al.  include sustainable management practices, given the somewhat indiscriminate use of insecticides to control RWA to date. They also include regular testing of field populations for evolution of insecticide resistance in their recommendations. To determine how RWA populations change over time annual monitoring was done from 2010 to 2019 in the wheat production areas of South Africa. The most recent observations is discussed here.
2. Material and methods
2.1 Survey and collection of RWA at landscape level
RWA samples were collected annually during the wheat growing season in South Africa from 2010 to 2019. All main wheat production areas within the known distribution of the RWA were sampled. The same areas were sampled each year and where possible the same fields (Figures 1 and 2). There are two main dryland wheat production areas in South Africa where RWA commonly occur, the Western Cape (winter rainfall area) (Figure 1) and the Free State (a summer rainfall area) (Figure 2), with irrigated wheat production areas in the Central and Western Free State and Northern Cape (Figure 2). Sampling sites were selected off primary or secondary roads that transected major wheat or barley production areas. Sites were 10-20 km apart with distances depending on the continuity of wheat fields. In the Western Cape an average of 32 fields were sampled (Figure 1) and in the Free State an average of 61 fields were sampled (Figure 2). Samples were collected from cultivated wheat, barley and oats as well as volunteer wheat, wild oats, rescue grass and false barley in road reserves and around cultivated fields. Infested leaves were placed in Petri dishes containing moist filter paper and stored in an icebox for transportation to the glasshouse. The number of aphids per plant, percentage plants infested, growth stage of the plants and damage on the plants were recorded. The geographical co-ordinates and elevation where the samples were collected were also captured on a GPS and all the information of each sample collected was entered into a database (Windows Office –Excel).
2.2 Establishing clone colonies of collected RWA samples
A single female aphid from each sample collected in the field was transferred to a wheat plant and caged (gauze size: 315micron) to produce a clone colony. RWA clone colonies are kept in glasshouse cubicles at night/day temperatures of 16 °C/22 °C and maintained on various wheat cultivars to avoid pre-adaptation to a specific cultivar until they multiplied sufficiently to be used for screening. Each clone colony is cultured for an average period of two to three months before screening.
2.3 Screening of clone colonies of collected RWA samples for determination of potential biotypes
The biotype of each RWA clone was determined by screening its feeding damage on 11 previously established plant resistant sources containing designated resistance genes
Ten seeds of each plant entry were planted in a seedling tray filled with sterilized sand in a randomized complete block design with four replications for each biotype determination. Plant entries were randomly assigned to rows and were separated by border rows planted with RWA susceptible Tugela. Plants were kept in glasshouse cubicles at night/day temperatures of 16 °C/22 °C, natural light. Immediately after planting, the seedling trays were placed in gauze (315micron) cages to avoid contamination by secondary aphids. Plants were infested at the two-leaf stage with collected RWA clone colonies. Plants were rated with a ten-point damage rating scale, which included leaf chlorosis and leaf rolling . A score from 1–4 describes leaf chlorosis, 5–6 striping on the leaves and 7–10 rolling. Once the susceptible wheat Tugela showed susceptible damage symptoms, all plants were rated. RWA biotypes were classified by using damage ratings for each plant entry where the plant was considered resistant (R) if the damage rating was 1–6.5 and susceptible (S) if the damage rating was above 6.5–10. Each clone was given a biotype designation based on the differential virulence profile to the
Biotype (clones) groups across all plant differentials were analyzed using a two-way (clone, plant entry) analysis of variance (ANOVA). Mean damage rate entries with significant (P < 0.05) clone-by-plant interactions were separated by Fisher’s protected least significant difference (LSD) test at the 5% level (SAS Institute 2003).
3. Results and discussion
Representative samples of five RWA biotypes were collected in the different wheat production areas in South Africa, with a range of different climatic conditions and different host plants from 2010 to 2019 (Figure 1 and Figure 2). The number of samples collected in a specific area varied depending on the area planted with wheat or barley or the availability of alternative hosts and the level of infestation. An average of 32 fields were sampled in the Western Cape (Figure 1) and 61 in the Free State (Figure 2). Environmental conditions, including temperature, humidity, rainfall, soil type and availability of host plants play an important role in the population increase and distribution of different RWA biotypes. Because these variables change from year to year and between different areas, the distribution of RWA biotypes will vary over years and between different geographical areas.
Analysis of the main effects of damage rating for the five Russian wheat aphid biotype colonies indicated a significant clone (F = 117.48; df = 3; P < 0.0001), plant entry (F = 133.59; df = 11; P < 0.0001) and clone-by-plant entry interaction (F = 12.82; df = 33; P < 0.0001), suggesting that the plant entries responded differently to the different aphid clones. Biotypes are identified by the distinct feeding damage responses they produce on wheat carrying different RWA resistance genes from
The concentration of RWA biotypes occurred mainly in the Eastern Free State with very few wheat fields infested with RWASA1 (original biotype, reported in 1978). RWASA1 occurred mainly in the Western Free State and Northern Cape. Since 2006, five distinct RWA biotypes have been recorded in the wheat production areas of the Eastern Free State, RWASA2 in 2006; RWASA3 in 2009; RWASA4 in 2011 and RWASA5 in 2018. The populations of RWA biotypes fluctuated over the years with RWASA2 being the dominant biotype from 2010 to 2011, RWASA3 dominating from 2012 to 2013 and RWASA4 from 2014 to 2016 (Figure 3). During the 2018 season RWASA5, was recorded for the first time on 8 wheat fields in the Lindley, Reitz and Danielsrus areas in the Eastern Free State. During 2019 this biotype had increased and spread to other areas of the Eastern Free State and was recorded on 12 wheat fields in the Eastern Free State. This biotype was dominant from 2018 to 2019 (Figure 3). Merrill et al.  found, in a general survey of aphid mixtures for virulence to resistant Yumar (with
Given the invasive ability, evolutionary adaptability to changing conditions, virulence, and fecundity of RWA, it remains a threat to global wheat production and wheat cultivation. RWA remain present in all the wheat production areas of South Africa and these populations are becoming more virulent as indicated by the spread of the recently recorded biotype, RWASA5, in the Eastern Free State. Management practices in different regions of South Africa may cause increased virulence in RWA populations. Based on these observations testing of field populations to understand if insecticide resistance is evolving in RWA populations in the Western Cape is warranted. It is important that future management practices focus on sustainability instead of the indiscriminate use of insecticides globally to control RWA to date. Increasing diversity in fields through undersowing, reduced tillage, intercropping and incorporation of cover crops will be an effective start to sustainable management practices. Vegetation strips have favorable microclimate for survival of generalist predators, and alternative prey and resources during winter, resulting in higher densities of generalist predators in cereal fields [40, 41]. This together with minimal use of insecticides, only when necessary, will increase the insects providing ecosystem services and predators, parasitoids and pathogens that will keep RWA populations and economical damage low. Management approaches against cereal aphid invasions differ depending on aphid ecology, specific system influences, and local management practices . Any practice based on aphid population monitoring that facilitates threshold-based insecticide use will be effective across agroecosystems, with area-wide management systems being most appropriate to large-scale cereal production systems.
The author wish to acknowledge the Agricultural Research Council (ARC)-Small Grain for facilities provided and the Winter Cereal Trust (WCT) for research funding.
Conflict of interest
The author declare no conflict of interest.