Responses of summer cereal aphid populations to reduced rate aphicide applications in field plots of winter wheat

Abstract 1 Recommended and reduced rate applications of pirimicarb and alpha‐cypermethrin were applied to winter wheat crops to control summer infestations of grain aphid (Sitobion avenae) and rose‐grain aphid (Metopolophium dirhodum). 2 Aphid numbers were assessed weekly and the yield response to treatment application was compared with accumulated aphid days on the crop. 3 Responses to aphicide treatment varied between sites according to variations in the subsequent development of aphid populations under varying weather conditions and differential pressures from aphid natural enemies. 4 Alpha‐cypermethrin treatment reduced spider density at most sites, and also resulted in a resurgence of aphid populations at three sites.     

Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators

Predation by generalist predators is difficult to study in the field because of the complex effects of positive and negative interactions within and between predator species and guilds. Predation can be monitored by molecular means, through identification of prey DNA within predators. However, polymerase chain reaction (PCR) amplification of prey DNA from predators cannot discriminate between primary and secondary predation (hyperpredation), in which one predator feeds on another that has recently eaten the target prey. Here we quantify, for the first time, the potential error caused by detection of prey DNA following secondary predation, using an aphid-spider-carabid model. First, the aphid Sitobion avenae was fed to the spider Tenuiphantes tenuis and the carabid Pterostichus melanarius, and the postconsumption detection periods, for prey DNA within predators, were calculated. Aphids were then fed to spiders and the spiders to carabids. Aphid DNA was detected in the predators using primers that amplified 245- and 110-bp fragments of the mitochondrial cytochrome oxidase I gene. Fragment size and predator sex had no significant effect on detection periods. Secondary predation could be detected for up to 8 h, when carabids fed on spiders immediately after the latter had consumed aphids. Beetles tested positive up to 4 h after eating spiders that had digested their aphid prey for 4 h. Clearly, the extreme sensitivity of PCR makes detection of secondary predation more likely, and the only reliable answer in future may be to use PCR to identify, in parallel, instances of intraguild predation.     

Density dependence in cereal aphid populations

Long sequences of data on the incidence of cereal aphids from five European countries were analysed for evidence of density dependent processes occurring between years. Using a randomisation test (Pollard, Lakhani & Rotheray, 1987), density dependence was revealed in all (16) population censuses of Metopolo-phium dirhodum , 60% of Rhopalosiphum padi censuses (10 of 17) but only 25% of Sitobion avenae population censuses (4 of 16). Correcting for density independent effects of weather revealed the existence of significant direct density dependence in some populations censuses where it was previously undetected. The implications of density dependence in cereal aphid populations are considered.     

Rapid screening of invertebrate predators for multiple prey DNA targets

DNA-based techniques are providing valuable new approaches to tracking predator-prey interactions. The gut contents of invertebrate predators can be analysed using species-specific primers to amplify prey DNA to confirm trophic links. The problem is that each predator needs to be analysed with primers for the tens of potential prey available at a field site, even though the mean number of species detected in each gut may be as few as one or two. Conducting all these PCRs (polymerase chain reactions) is a lengthy process, and effectively precludes the analysis of the hundreds of predators that might be required for a meaningful ecological study. We report a rapid, more sensitive and practical approach. Multiplex PCRs, incorporating fluorescent markers, were found to be effective at amplifying degraded DNA from predators' guts and could amplify mitochondrial DNA fragments from 10+ species simultaneously without 'drop outs'. The combined PCR products were then separated by size on polyacrylamide gels on an ABI377 sequencer. New primers to detect the remains of aphids, earthworms, weevils and molluscs in the guts of carabid predators were developed and characterized. The multiplex-sequencer approach was then applied to field-caught beetles, some of which contained DNA from as many as four different prey at once. The main prey detected in the beetles proved to be earthworms and molluscs, although aphids and weevils were also consumed. The potential of this system for use in food-web research is discussed.     

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.     

Geographic and microgeographic genetic differentiation in two aphid species over southern England using the multilocus (GATA)4 probe

Samples of the grain aphid Sitobion avenue (F.) and the rose-grain aphid Metopolophium dirhodum (Walker) were collected in late March from wheat fields and adjacent road-side grasses at a number of locations in southern England. Unparasitized aphids were DNA fingerprinted using the multilocus (GATA)₄ probe. Over all locations, the fingerprints of individual S. avenue caught in wheat had lower overall average distances of band migration (ADBM) and shared a higher proportion of bands, than fingerprints of individuals caught in adjacent road-side grasses. The ADBM of fingerprints of S. avenue collected on road-side grasses altered significantly with geographical location, while the ADBM of fingerprints of S. avenue caught on wheat did not. A comparison of the fingerprints of individual M. dirhodum caught in wheat and neighbouring road-side grasses did not reveal any genetic differentiation. Fingerprints of M. dirhodum that were caught in the same host type did however, show significant variation in ADBM between different locations. With both S. avenue and M. dirhodum, spatial autocorrelation revealed that locations that were close together were no more likely to have individuals with similar ADBM than locations mat were far apart Our results suggest that (i) particular clones of S. avenue prefer to colonize wheat; and/or that (ii) particular clones of S. avenae perform better on wheat man other clones. It is unclear why M. dirhodum did not show any genetic structuring according to host type, but this species appears to engage in sexual reproduction much more frequently than S. avenae in southern England. M. dirhodum is likely to have displayed genetic heterogeneity between locations either because of founder effects, or because of genetic drift.     

The significance of facultative scavenging in generalist predator nutrition: detecting decayed prey in the guts of predators using PCR

Gut-content analyses using molecular techniques are an effective approach to quantifying predator-prey interactions. Predation is often assumed but scavenging is an equally likely route by which animal DNA enters the gut of a predator/scavenger. We used PCR (polymerase chain reaction) to detect scavenged material in predator gut homogenates. The rates at which DNA in decaying slugs (Mollusca: Pulmonata) and aphids (Homoptera: Aphididae) became undetectable were estimated. The detectability of DNA from both carrion types in the guts of the generalist predator Pterostichus melanarius (Coleoptera: Carabidae) was then determined. The effects of carrion age and weight, as well as beetle sex, on detection periods, were quantified. Laboratory trials measured prey preference of beetles between live and decaying prey. Further experiments measured, for the first time, feeding by P. melanarius on dead slugs and aphids directly in the field. In both field and laboratory, P. melanarius preferentially fed on dead prey if available, but preference changed as the prey became increasingly decayed. Disappearance rates for slug carrion in wheat fields and grasslands were estimated and P. melanarius was identified as the main scavenger. Comparison of the retention time for dead slugs in the field, with the detection period for decaying slug material in the guts of the predators, showed that PCR-based techniques are not able to distinguish between predated and scavenged food items. This could potentially lead to overestimation of the impact of predation on slugs (and other prey) by carabids. Possible implications of facultative scavenging by invertebrate predators for biocontrol and food-web research are discussed.     

Development of selective aphicide treatments for integrated control of summer aphids in winter wheat

Field experiments on the use of recommended and reduced application rates of aphicides for control of summer aphid infestations on winter wheat have been done at five sites each year from 1990 to 1992. The experiment compared sprays of pirimicarb at recommended rate (140g a.i. ha^-1) and reduced rate (25 g a.i. ha^-1) and of alphacypermethrin at recommended rate (15 g a.i. ha^-1) and one third recommended rate (5 g a.i. ha^-1), each applied either at flag leaf emergence or at flowering. Aphid infestations were allowed to develop naturally and were measured at critical growth stages. In 1990, overwintered aphid infestations, together with established populations of parasitoids, were detected at four of the five sites when the first assessment was made in April. Parasitoids provided sufficient aphid control to prevent yield loss at two sites, without pesticide applications. At three sites both aphicides gave similar levels of control and yield response at both recommended and reduced application rates. In 1991 and 1992 no overwintered aphids were detected in the crops and aphid infestations developed much later. Aphicide applications gave significant yield responses at four sites in 1992. Recommended rates gave better control of aphids than reduced rates. There was no significant difference in the yield response obtained with different rates of aphicide.     

The effects of organic and conventional fertilizers on cereal aphids and their natural enemies

• 1 Aphids are important pests of spring cereals and their abundance and the impact of their natural enemies may be influenced by fertilizer regime.
• 2 We conducted a 2‐year field study investigating the effects of organic slow‐release and conventional fertilizers on cereal aphids, hymenopteran parasitoids and syrphid predators and considered how the effects of fertilizers on barley morphology and colour might influence these species.
• 3 Barley yield was greater in conventionally fertilized pots. Barley morphology was also affected by treatment: vegetative growth was greater under conventional treatments. Barley receiving organic fertilizers or no fertilizer was visually more attractive to aphids compared with plants receiving conventional fertilizers.
• 4 Aphids were more abundant in conventionally fertilized barley but the reason for this increased abundance was species specific. Metopolophium dirhodum was responding to fertilizer effects on plant morphology, whereas Rhopalosiphum padi was sensitive to the temporal availability of nutrients.
• 5 Syrphid eggs were more numerous in conventionally fertilized pots, whereas the response of parasitoids appeared to be dependent on the abundance of aphids, although the number of parasitoid mummies was low in both years.
• 6 This research shows that the fertilizer treatment used can affect numerous characteristics of plant growth and colour, which can then influence higher trophic levels. This knowledge might be used to make more informed fertilizer application choices.

     

Feeding responses of carabid beetles to dimethoate-contaminated prey

Abstract 1 The feeding responses of Pterostichus madidus Fab., P. melanarius Illiger and Nebria brevicollis Fab. (Coleoptera: Carabidae) to dimethoate‐contaminated prey were investigated in ‘no‐choice’ and ‘choice’ feeding tests. 2 In the no‐choice tests, starved beetles were presented with aphid prey treated with four concentrations of dimethoate. In the choice tests, treated and untreated prey were presented together and the feeding preferences of the starved beetles observed. 3 No avoidance or rejection behaviour was seen in any of the carabids in either of the tests, i.e. no discrimination of the treated and untreated prey was observed. 4 Sufficient dimethoate was consumed with the aphid prey to cause significant mortality levels in the carabids. 5 The concentrations of dimethoate used in these experiments are comparable to field exposure, so carabids feeding in treated fields and field margins could potentially suffer lethal effects via the indirect exposure route of consuming contaminated prey.     

A field evaluation of different criteria for determiningthe need to treat winter wheat against the grain aphid Sitobion avenae and the rose-grain aphid Metopolophium dirhodum

The economics of control of grain aphid (Sitobion avenae) and rose-grain aphid (Metopolophium dirhodum) were investigated in a series of experiments carried out across England in 1988 and 1989. Sprays of pirimicarb or dimethoate were applied at three growth stages and yield effects measured. Aphid infestations were determined by a range of different methods, to evaluate the value of each for decision making. Aphids overwintered in crops in mild conditions in both seasons, resulting in early population build-up and decline in many cases. Aphicide sprays applied during the booting stage increased average yields by 0.26 t/ha. Profitability of the treatment strategies considered was not greatly enhanced by selective spray application related to aphid assessment at this stage. Delaying decision making to the flowering or grain-filling stages resulted in reduced profitability. A poor correlation between aphid numbers and crop yield response to sprays was found. This was shown to be due to differences in subsequent aphid population development and in aphicide efficacy. Grain quality was affected only by high aphid infestations which caused large yield reductions.     

Population dynamics of cereal aphids: influence of a shared predator and weather

1 Aphid populations may show strong year-to-year fluctuations, but questions remain regarding the dominance of factors that cause this variation, especially the role of natural enemies. To better understand the dynamics of aphid species that occur as pests in cereals, we investigated the relative influence of top-down control by a predator and weather (temperature and precipitation) on population fluctuations of three cereal aphid species.
2 From 1987 to 2005, populations of Metopolophium dirhodum , Sitobion avenae and Rhopalosiphum padi in insecticide-free stands of winter wheat were monitored in the Praha-Ruzyné region of the Czech Republic. Densities of an aphidophagous predator, the ladybeetle Coccinella septempunctata , were recorded from an overwintering site in the landscape. Weather was quantified using historical records.
3 A significant bottom-up effect of densities of aphids on those of C.   septempunctata was found, but evidence of direct top-down regulation of aphids by C.   septempunctata was only significant in the case of R.   padi . There was no significant periodicity in the dynamics of the aphid or C.   septempunctata , suggesting that there was no clear predator-prey cycle. Combinations of C.   septempunctata and weather variables could be used to explain M.   dirhodum and R.   padi per capita rate of change. There were also indications that weather directly affected peak density of M.   dirhodum .
4 We conclude that regional estimates of C.   septempunctata densities are not sufficient to determine whether aphid population dynamics are driven by predator–prey interactions. Feasibility of time series analysis as an investigative tool in aphid population dynamics studies is discussed.     

Aphid colony turn‐over influences the spatial distribution of the grain aphid Sitobion avenae over the wheat growing season

1 Temporary habitats are characterized by the appearance and disappearance of patches in which resources are available for a limited period only. Organisms living in those environments usually exhibit adaptive traits, such as a high ability to find and exploit new patches. Among them are phytophagous insects, such as crop pests living in agroecosystems. Understanding how phytophagous insects invade a new patch is of great agricultural importance. 2 Here, we investigated how aphids colonize a wheat field by studying the spatial and temporal dynamics of their populations at large (field) and fine (group of host plants) scales. 3 The sampling design consisted of counting and locating aphid colonies within 30 0.25 m² squares randomly spaced in a 1.5‐ha winter wheat field over 2 months. All colonies were precisely located within the squares and their composition in terms of morphs was determined. 4 We show that: (i) immigration of winged aphids was a major factor driving the aphid population dynamics during a large part of the season and (ii) within the field, populations established late in the growing season. Aggregated, populations of aphids became progressively homogeneously distributed at the field scale. At the scale of a 0.25 m² square, infested plants were clustered in randomly distributed small patches, and aphid colonies experienced high extinction rates, suggesting failure in population establishment. 5 Because immigration may considerably influence both population dynamics and spatial distribution, our study suggests that future predictive models should give a greater weight to spring immigrants.     

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.     

Effects of Aphid Prey on Larval Development and Mortality of Adalia bipunctata and Coccinella septempunctata (Coleoptera: Coccinellidae)

Developmental time and mortality rate of Adalia bipunctata (L.) and Coccinella septempunctata L. (Coleoptera: Coccinellidae) were determined when feeding on five aphid species. Metopolophium dirhodum (Walker), Sitobion avenae (F.), Rhopalosiphum padi (L.), Hyalopterus pruni (Geoffr.) and Myzus cerasi F. (Homoptera: Aphididae) are widespread in Tekirda?, Turkey. Tests were carried out in a controlled environmental chamber (25±1°C temperature, 65±5% relative humidity and 16 h light:8 h dark period). Developmental times for A. bipunctata and C. septempunctata larvae varied significantly depending on species of aphid prey (P<0.05). Development time (±S.E.) varied from 17.50±0.84 to 20.83±1.60 days for C. septempunctata and 16.7±0.76 to 20.7±1.03 days for A. bipunctata. Mortality of A. bipunctata (50%) and C. septempunctata (63%) were highest on H. pruni.