Comparing growth patterns among field populations of cereal aphids reveals factors limiting their maximum abundance

Cereal stands in central Europe are commonly infested with three species of aphids that may become serious pests. With increasing abundance, the proportion of a particular species in the total aphid population may remain constant, suggesting a density-independent exponential growth, or the proportion can change, suggesting density-dependent constraints on growth. The constraints that affect particular species, and thus their relative abundance, were studied. The proportionality between maximum abundances of the cereal aphids was studied using a 10-year census of the numbers of aphids infesting 268 winter wheat plots. For two species their abundance on leaves and ears was compared. With increasing aphid density the maximum abundance of Rhopalosiphum padi (Linnaeus) remained proportional, but not that of Sitobion avenae (Fabricius), which was constrained by the smaller surface area of ears compared to leaves. There was no evidence of inter-specific competition. Maximum abundance of R. padi and Metopolophium dirhodum (Walker) on leaves did not change proportionally as the proportion of M. dirhodum decreased with increasing overall aphid density. This decrease was probably caused by the restricted distribution of M. dirhodum, which is confined to leaves, where space is limiting. No change in proportion between populations was detected when the average densities were below 0.54 aphids per leaf or ear. Non-proportional relationships between aphid populations appeared to be due to spatial constraints, acting upon the more abundant population. Detecting the limitation of population growth can help with the assessment of when density-independent exponential growth is limited by density-dependent factors. This information may help in the development of models of cereal aphid population dynamics.     

Methods of Recording Aphid Populations for Use in Research on Potato Virus Diseases

Methods of counting aphids infesting potato crops are reviewed and discussed. The results of an aphid survey in different parts of England during 1946 and of counts at Rothamsted during 1947 are given and used to illustrate methods of expressing the counts; the extent of virus spread in 1946 showed no close correlation with aphid numbers. It is concluded that an estimate of the number of aphids per plant is better for virus disease research than the number per 100 leaves. A method of estimating the number of aphids per plant with tolerable accuracy is described, but it is concluded that for most surveys a method which does not necessitate the counting of the aphids is adequate. Such a method, based on the percentage of leaves infested, is described.     

The effects of temperature and host quality on the rate of increase of the grain aphid (Sitobion avenae) on wheat

From 10°C to 25°C Sitobion avenae reared on wheat developed faster, had a higher mean relative growth rate and a higher intrinsic rate of increase on ears than on the flag leaves. At temperatures above 25°C there is a marked decline in the performance of the aphid. The intrinsic rate of increase is strongly correlated with the mean relative growth rate during development for both aphids reared on ears and flag leaves from 10°C to 25°C.     

Large‐scale migration synchrony between parasitoids and their host

1. Parasitoids are a valuable group for conservation biological control. In their role as regulators of aphid pests, it is critical that their lifecycle is synchronised with their hosts in both space and time. This is because a synchronised parasitoid community is more likely to strengthen the overall conservation biological control effect, thus damping aphid numbers and preventing potential outbreaks. One component of this host–parasitoid system was examined, that of migration, and the hypothesis that peak summer parasitoid and host migrations are synchronised in time was tested. 2. Sitobion avenae Fabricius and six associated parasitoids were sampled from 1976 to 2013 using 12.2‐m suction‐traps from two sites in Southern England. The relationship between peak weekly S. avenae counts and their parasitoids was quantified. 3. Simple regression models showed that the response of the peak parasitoids to the host was positive: generally, more parasitoids migrated with increasing numbers of aphids. Further, when averaged over time, the parasitoid migration peak date corresponded with the aphid migration peak. The co‐occurrence of the peaks was between 51% and 64%. However, the summer peak in aphid migration is not steadily shifting forward with time unlike spring first flights of aphids. Cross‐correlation analysis showed that there were no between‐year lagged effects of aphids on parasitoids. 4. These results demonstrate that the peak in migration phenology between host and parasitoid is broadly synchronised within a season. Because the threshold temperature for flight (> 12 °C) was almost always exceeded in summer, the synchronising agent is likely to be crop senescence, not temperature. Studies are needed to assess the effects of climate change on the mismatch potential between parasitoids and their hosts.     

The influence of nitrogen fertiliser on the population development of the cereal aphids Sitobion avenae (F.) and Metopolophium dirhodum (Wlk.) on field grown winter wheat

The effect of nitrogen fertiliser on populations of the cereal aphids Sitobion avenae and Metopolophium dirhodum on winter wheat was investigated in a three year field experiment. Naturally occurring aphid populations were monitored on three nitrogen treatments; none, nitrogen application using Canopy Management guidelines (130–210 kg ha^-1) and conventional practice (190 kg ha^-1). Inoculations of laboratory reared S. avenae were used to enhance field populations on half the plots. Natural populations of M. dirhodum remained below the current UK spray threshold level of two-thirds of shoots infested at the start of flowering, or five aphids per shoot in all years, whilst populations of S. avenae exceeded the threshold in all years. The response of the two species to nitrogen differed. Significantly higher populations of M. dirhodum were recorded in both treatments which received nitrogen in all years, whilst the response of S. avenae varied between years. In 1994 and 1995 when environmental conditions favoured aphid development, higher populations were recorded in the two treatments which received nitrogen. In 1993 when high rainfall created unfavourable conditions, higher populations were recorded in the plots receiving no nitrogen. Differences in peak density and cumulative aphid index of S. avenae resulted from differences in the rate of population increase between ear emergence and peak density on the different treatments. Populations prior to ear emergence were higher in the plots which received nitrogen but the differences were not statistically significant. There was no evidence of a difference in the timing of population decline in the different treatments. In 1993 higher levels of infection by entomopathogenic fungi were observed in all treatments. Significantly higher levels of infection were recorded in the treatments receiving nitrogen, which may have accounted for the lower S. avenae populations recorded. It is possible that the larger canopies recorded in these treatments produced conditions which favoured infection by fungi, thereby limiting aphid population growth. The results indicate that application of nitrogen increases natural populations of M. dirhodum, and under favourable conditions, populations of S. avenae. However, in suboptimal climatic conditions, the application of nitrogen fertiliser can lead to lower populations of 5. avenae. The data also suggest that there is no consistent difference between a conventional and Canopy Managed approach to nitrogen fertiliser use in terms of the risk of infestation by cereal aphids.     

Comparison of the potential rate of population increase of brown and green color morphs of Sitobion avenae (Homoptera: Aphididae) on barley infected and uninfected with Barley yellow dwarf virus

Life tables of brown and green color morphs of the English grain aphid, Sitobion avenae (Fabricius) reared on barley under laboratory conditions at 20 ± 1°C, 65% ± 5% relative humidity and a photoperiod of 16 : 8 h (L : D) were compared. The plants were either: (i) infected with the Barley yellow dwarf virus (BYDV); (ii) not infected with virus but previously infested with aphids; or (iii) healthy barley plants, which were not previously infested with aphids. Generally, both color morphs of S. avenae performed significantly better when fed on BYDV‐infected plants than on plants that were virus free but had either not been or had been previously infested with aphids. Furthermore, when fed on BYDV‐infected plants, green S. avenae developed significantly faster and had a significantly shorter reproductive period than the brown color morph. There were no significant differences in this respect between the two color morphs of S. avenae when they were reared on virus‐free plants that either had been or not been previously infested with aphids. These results indicate that barley infected with BYDV is a more favorable host plant than uninfected barley for both the color morphs of S. avenae tested, particularly the green color morph.     

Effect of three isolates of Pandora neoaphidis from a single population of Sitobion avenae on mortality,speed of kill and fecundity of S. avenae and Rhopalosiphum padi at different temperatures

We studied the effect of three Pandora neoaphidis isolates from one Sitobion avenae population, three temperatures, and two aphid species namely S. avenae and Rhopalosiphum padi on (i) aphid mortality, (ii) time needed to kill aphids, and (iii) aphid average daily and lifetime fecundity. A total of 38% of S. avenae and 7% of R. padi died and supported fungus sporulation. S. avenae was killed 30% faster than R. padi. Average daily fecundity was negatively affected only in S. avenae inoculated with, but not killed by, P. neoaphidis. Nevertheless, lifetime fecundity of both aphid species inoculated and sporulating with P. neoaphidis was halved compared to lifetime fecundity of surviving aphids in the control. Increased temperature resulted in higher mortality rates but did not consistently affect lethal time or fecundity. Results suggest that (i) temperature effects on virulence differ between isolates, even when obtained within the same host population, and (ii) even though an isolate does not kill a host it may reduce its fecundity. Our findings are important for the understanding of P. neoaphidis epizootiology and for use in pest-natural enemy modelling.     

Silencing the expression of the salivary sheath protein causes transgenerational feeding suppression in the aphid Sitobion avenae

Aphids produce gel saliva during feeding which forms a sheath around the stylet as it penetrates through the apoplast. The sheath is required for the sustained ingestion of phloem sap from sieve elements and is thought to form when the structural sheath protein (SHP) is cross‐linked by intermolecular disulphide bridges. We investigated the possibility of controlling aphid infestation by host‐induced gene silencing (HIGS) targeting shp expression in the grain aphid Sitobion avenae. When aphids were fed on transgenic barley expressing shp double‐stranded RNA (shp‐dsRNA), they produced significantly lower levels of shp mRNA compared to aphids feeding on wild‐type plants, suggesting that the transfer of inhibitory RNA from the plant to the insect was successful. shp expression remained low when aphids were transferred from transgenic plants and fed for 1 or 2 weeks, respectively, on wild‐type plants, confirming that silencing had a prolonged impact. Reduced shp expression correlated with a decline in growth, reproduction and survival rates. Remarkably, morphological and physiological aberrations such as winged adults and delayed maturation were maintained over seven aphid generations feeding on wild‐type plants. Targeting shp expression therefore appears to cause strong transgenerational effects on feeding, development and survival in S. avenae, suggesting that the HIGS technology has a realistic potential for the control of aphid pests in agriculture.     

Aphid flight and change in abundance of winter wheat pests

Composition, dominance and change in population density of species flying over and feeding on winter wheat fields was studied between 1982 and 1998 at Mosonmagyaróvár. There were 29 aphid species among flying insects. The ones imposing risk to winter wheat were as follows: Diuraphis noxia Kurdj., Metopolophium dirhodum Walk., Rho‐palosiphum padi L., Schizaphis graminum Rond., Sitobion avenae Fabr. Number of flying individuals changed year by year, depending principally on climatic factors (temperature, relative humidity, and rainfall). Flight was continuous from late April to harvest. In the average of 17 years flight peak was observed in June.

Establishment of the firsts alate individuals of aphids with holocyclic development can be expected from the second decade of April. As a result of the continuous reproduction, the peak in number of individuals was observed in the second decade of June. During the six years between 1993 and 1998 this value was 17.18 aphids/ plant. Every year there were deviations from the average data, e.g., in 1994 aphid number per plant was 33.61. These pests appeared on the ears in the first decade of June, their number was continuously increasing due to drying of leaves.

During the six years when detailed data were recorded, Rh. padi L. was the dominant species three times (1994: 70.4%; 1995: 82.6%; 1996: 87.9%), M. dirhodum Walk. took this role two times (1993: 67.1%; 1997: 84.8%) and S. avenae Fabr. only once (1998: 53%).

Considering seventeen years’ data, it is necessary to produce resistant varieties and/or seed dressing, or insecticide treatment to control the first alates.     

高压静电场对小麦叶片保护酶系统及麦长管蚜种群动态的影响

为明确高压静电场胁迫小麦种子对其叶片以及麦长管蚜Sitobion avenae Fabricius产生的影响。测定了小麦苗期叶片及麦长管蚜体内抗氧化酶(SOD,POD,CAT)的活性,并采用盆栽种群实验研究了麦长管蚜的种群动态。实验结果表明:(1)在未被麦长管蚜取食的小麦叶片中,SOD和POD活性最大值均出现于4 k V/cm处理组,且与对照组差异显著(P0.05),CAT活性在未被取食的叶片中无显著差异(P0.05);而被取食过的叶片中,4 k V/cm处理组的SOD和POD活性均显著低于对照组(P0.05),而CAT活性结果显示4 k V/cm和6 k V/cm处理组均显著低于对照组(P0.05)。(2)静电场处理组中麦长管蚜的SOD和CAT活性均显著高于对照组(P0.05),但POD活性均显著低于对照组(P0.05)。(3)种群动态和逻辑斯蒂模型参数显示4 k V/cm处理组的小麦环境容纳量(K)最小。研究的创新点在于对影响麦长管蚜的介质(小麦)的抗氧化酶活性进行了测定,进一步明确了高压静电场对动植物的影响,说明了4 k V/cm是影响小麦和麦长管蚜的关键强度,为高压静电生态控蚜提供了新思路。     

Farm‐scale assessment of movement patterns and colonization dynamics of the grain aphid in arable crops and hedgerows

1 Integrated management of crop pests requires the identification of the appropriate spatial scale at which colonization processes occurs. We assessed, by coupling demographic and genetic methods, the relative contribution of local and transient migrants of the grain aphid Sitobion avenae to wheat field colonization in spring. 2 We examined, during two consecutive years, the daily colonization of wheat by aphid migrants and compared this with daily aphid flight monitored by a local 12.2‐m suction trap. The genetic profiles of aphids landing on crops were compared with those of both flying aphids caught by the suction trap and local populations from arable crops and hedgerows. 3 In the first year, we observed: (i) a strong correlation between aphids colonizing the crop and those moving within the crop and a close genetic similarity between aphids from these samples and (ii) a high level of genetic differentiation between these aphids and populations from local cereals and field margins. In the second year, the number of migrants recorded on the wheat was three‐fold higher than in the previous year, and less correlated with that recorded by the suction trap. This was associated with a lack of genetic differentiation between all samples. 4 This variation in the colonization processes resulted mainly in an abrupt increase in abundance of genotypes from local over‐wintering sites in 2004. This suggests that, despite the long range dispersal potential of the grain aphid, outbreak risks could be mainly determined at a local scale, encouraging the design of relatively small management units.     

The effect of barley yellow dwarf virus on honeydew production by the cereal aphids, Sitobion avenae and Metopolophium dirhodum

Individual S. avenae and M. dirhodum excreted significantly fewer droplets of honeydew on plants infected with BYDV than on healthy plants. S. avenae excreted less honeydew on the ears than on the leaves of wheat. M. dirhodum excreted less than S. avenae on the leaves. The size of honeydew droplets increased with the age of aphids but was not affected by BYDV infection. Possible reasons for the observed effects of BYDV on honeydew excretion are discussed.     

The role of awns in the resistance of cereals to the grain aphid, Sitobion avenae

Six genotypes of awned spring wheat were more resistant to Sitobion avenae than de-awned wheat. Aphids that fed on awns were up to 22% less fecund and were more likely to be dislodged than aphids that fed elsewhere on an ear. These two factors reduced aphid population growth on awned earing plants in the field to a third of that observed on awnless plants. As awns may also benefit yield and are easy to select for it is recommended that awned winter wheats could be bred and used to reduce the incidence of outbreaks of S. avenae.     

Host plant age and population development of a cereal aphid, Metopolophium dirhodum (Hemiptera: Aphididae)

The sudden decline following the peak in population abundance of aphids on crops of small grain cereals is attributed to the joint effect of natural enemies and plant senescence. To distinguish between these causes, a four year experiment was established in which the numbers of Metopolophium dirhodum (Walker) infesting spring wheat plots sown from April to June at c. 14 day intervals were determined. Aphid abundance in replicates sown at successive dates peaked within a period of 5-9 days (106-171 day degrees above a base temperature of 0 degrees C) although their sowing dates varied by 62-97 days (727-1106 day degrees). At the time of the aphid population peaks, plants in the different sowings differed in age (11-99 days), developmental stage (stage 15-65 on the Zadoks scale), leaf nitrogen content and shoot mass. Maximum abundance of M. dirhodum decreased with sowing date because the time available for its population increase was shorter on late than early sowings. The abundance of M. dirhodum on spring wheat was similar to its abundance on winter wheat. After reaching peak abundance, aphids declined in numbers within 3-7 days. The effect of host plant ageing on the M. dirhodumdecline thus appeared small. Natural enemies (largely mycoses), and timing of alata production may have contributed to the aphid decline.     

The effect of augmenting grain aphid (Sitobion avenae) numbers in a field of winter wheat in spring on the aphid's abundance in summer and its relevance to the forecasting of outbreaks

Sitobion avenae was introduced into areas within a field of winter wheat in Norfolk in mid-May 1985, when the indigenous population was negligible. Aphid numbers in these areas increased for the first 3 wk and declined for the next 4. A second S. avenue introduction into the same areas and into previously uninfested areas was carried out 5 wk after the first introduction, when the crop was at ear emergence complete (G.S. 59). This increased aphid numbers in the previously uninfested areas, but numbers in the previously infested areas continued to decline to below the level in control areas during the subsequent 2 wk. Populations in all areas then increased rapidly to a maximum, followed by a rapid final decline. Monitoring of the aphid and natural enemy populations, and caging aphids onto the crop, revealed that the principal cause of the population decline around G.S. 59 was predation by syrphids. The relevance of these findings to the problem of forecasting S. avenae outbreaks is discussed, and a general explanation for cereal aphid outbreaks is put forward.     

Common facultative endosymbionts do not influence sensitivity of cereal aphids to pyrethroids

1. Cereal aphids, including the bird cherry-oat aphid, Rhopalosiphum padi, and the grain aphid, Sitobion avenae, can transmit viruses that significantly reduce crop yields. To mitigate against yield losses, insecticides are routinely used to manage aphid populations.
2. Aphids can form relationships with endosymbionts that confer fitness benefits or consequences to the aphid. Recent artificial inoculation experiments indicate that endosymbionts could increase aphid susceptibility to insecticides, but this has not been explored using aphid populations naturally infected with endosymbionts.
3. Here, we sampled aphids from an important cereal production region in Lower Saxony, Germany. We characterized the endosymbiont profile of these aphid populations and conducted pyrethroid dose–response assays to test the hypothesis that facultative endosymbionts increase aphid susceptibility to insecticides.
4. We find that the level of insecticide susceptibility is highly variable in S. avenae and we identify populations that are sensitive and tolerant to pyrethroids, including populations collected from the same field. For R. padi, we find evidence for decreased sensitivity to pyrethroids, representing the first report of reduced sensitivity to pyrethroids in R. padi sampled from Central Europe.
5. We detected high endosymbiont infection frequencies in the aphid populations. 84% of aphids carry one facultative endosymbiont and 9% of aphids carry two facultative endosymbionts. We detected associations with Regiella insecticola, Fukatsia symbiotica, and Hamiltonella defensa. However, we do not identify a link between endosymbiont infection and insecticide susceptibility, indicating that other factors may govern the development of insecticide resistance and the need for alternative management strategies.

     

Predator density manipulation and its effects on populations of Rhopalosiphumpadi (Horn.: Aphididae) in spring barley

Experiments were carried out in 1981-83 to assess the impact of polyphagous predators (e.g. Carabidae, Staphylinidae and Araneae) on populations of cereal aphids in spring barley in Sweden. Barriers were erected around mid-field and field-edge plots at different times during the aphids' establishment phase in order to manipulate the predation pressure during the aphid pre-peak period; predators were emigrating from field boundaries. Rhopalosiphum padi was the dominant species of cereal aphid in 1981 and 1982, and was abundant in both years. Reduction of the predation pressure resulted in R. padi populations that were two to six times larger compared with those in unenclosed control plots. Aphid populations were much larger when the predation pressure was reduced earlier in June than when this was done later, in both years, since late erection of barriers excludes fewer predators because most had already entered the enclosed areas. In 1983, R. padi and Sitobion avenae were equally common but occurred in low numbers, and the effects of reducing the predation pressure were less obvious. Bembidion spp. (B. lampros and B. quadrimaculatum) and linyphiid spiders were the most abundant predators during the early establishment phase of aphid populations in each year, and significant inverse correlations were found between peak numbers of R. padi per shoot and numbers of predators from these taxa in 1981 and 1982. Similar relationships were found between total aphids and numbers of Staphylinidae, B. quadrimaculatum and Coccinella septempunctata in 1983. It was concluded that differences between the manipulated numbers of polyphagous predators caused the observed differences in peak population levels of R.padiin 1981,1982 and to a lesser extent, 1983. Apparent levels of parasitism and fungal disease were low during the pre-peak period. Aphid specific predators, abundant after the peak, were considered partly responsible for the decline of aphid populations each year. The results are compared with those from similar experiments elsewhere with S. avenae and Metopolophium dirhodum in winter wheat. Reasons why the effects of polyphagous predators are greater, and occur over a much shorter period of time in Sweden are discussed.     

Determination the population trends of cereal aphids and associated parasitoids by yellow sticky traps with reference to aphid management on wheat

Population trends of cereal aphids and their associated parasitoids inhabiting wheat plantations were monitored by yellow sticky traps. The identified aphids exhibited one seasonal peak for each and were found to be active during the first half of March. Data revealed that, Rhopalosiphum padi L peak occurred one week later than both of Schizaphis graminum (Rondani) and Rhopalosiphum maidis (Fitch). The numbers of aphid complex was recorded more at 90 than at 30 and 60 cm height. Hymenopterous parasitoids activity is synchronised with aphid species, whereas they appeared in small numbers at early and late wheat season and showed their peak on March, with a positive correlation coefficient with aphid populations. The tested compounds (Karate, Biscaya, Match 5% EC, Tracer 24% SC and Neem Azal T/S) showed 100% reduction in aphid numbers after 24 h post application. However, the general reduction percentages indicated 99.31 > 98.32 > 97.97 > 97.06 > 95.66%, by using the abovementioned compounds, respectively.     

Effects of Collembola and fertilizers on plant performance (Triticum aestivum) and aphid reproduction (Rhopalosiphum padi)

Effects of Collembola (Protaphorura fimata) on the development of wheat (Triticum aestivum) and the reproduction of aphids (Rhopalosiphum padi) were investigated at different soil nutrient concentrations in a laboratory experiment. Fertilization with N and NPK increased biomass and nitrogen content of wheat, aphid reproduction and abundance of Collembola. Presence of Collembola tended to decrease biomass of leaves and ears, and caused a delayed ear production of the plants. Aphid reproduction was significantly reduced in the presence of Collembola (−14%) and most pronounced in fertilizer treatments. We suggest that the reduction of aphid reproduction is caused by Collembola-mediated changes in resource allocation and growth of wheat.