Glyphosate applied to genetically modified herbicide-tolerant sugar beet and 'volunteer' potatoes reduces populations of potato cyst nematodes and the number and size of daughter tubers

Glyphosate, applied early or later or twice to genetically modified glyphosate‐tolerant sugar beet, gave excellent control of planted ‘volunteer’ potatoes growing within the crop compared to conventional herbicide programmes with or without clopyralid. In three out of four trials, this resulted in significant reductions in the numbers of eggs and cysts of potato cyst nematodes (Globodera rostochiensis and G. pallida) where infestations were moderate (23–89 eggs g^?1 soil). In the fourth trial, which had very high initial populations (130 eggs ^?1 soil), none of the herbicide treatments had any significant effect on numbers of nematode eggs or cysts. This was probably due to competition for feeding sites, and the early death of the potatoes in all treatments caused by feeding damage by the nematodes and infection by blight, which prevented the nematodes from completing their life cycle. Glyphosate also significantly reduced the number and size of daughter tubers produced, thus helping to prevent a further volunteer problem in the next crop in the rotation. This was achieved by one or two applications of one chemical compared to 2–5 applications of cocktails of conventional herbicides.     

Effects of Initial Nematode Density on Population Dynamics of Globodera rostochiensis on Resistant and Susceptible Potatoes

The influence of resistant and susceptible potato cultivars on Globodera rostochiensis population density changes was studied at different nematode inoculum levels (Pi) in the greenhouse and field. Soil in which one susceptible and two resistant cultivars were grown and fallow soil in pots was infested with cysts to result in densities of 0.04-75 eggs/cm³ soil. A resistant cultivar was grown in an infested field with Pi of 0.7-16.7 eggs/cm³ soil. Pi was positively correlated with decline of soil population densities due to hatch where resistant potatoes were grown in the greenhouse and in the field but not in fallow soil. However, Pi was not correlated with in vitro hatch of G. rostochiensis cysts in water or potato root diffusate. Under continuous culture o f a resistant cultivar, viable eggs per cyst declined 60-90% per plant growth cycle (4 weeks) and the number of cysts containing viable eggs had decreased by 77% after five cycles. The rate of G. rostochiensis reproduction on both resistant and susceptible cultivars was negatively correlated with Pi. These data were used to predict the effect of resistant and susceptible potato cultivars on G. rostochiensis soil population dynamics.     

Effects of Inoculum Density and Egg Age on Establishment of Globodera rostochiensis Populations

The establishment of Globodera rostochiensis Rol populations was examined under greenhouse conditions. The probability of G. rostochiensis population establishment was calculated from the number of plants that produced new cysts with viable eggs following inoculation with various numbers of eggs of different ages. Probability of population establishment was positively correlated with inoculum density but was not affected by the age of eggs used in these experiments. The probability of G. rostochiensis establishment ranged from 5% at densities of 2 eggs/pot to 100% at densities of 25 eggs/pot or greater. At densities of 3 eggs/pot and beyond, there was no correlation between inoculum density and the number of viable eggs/new cyst. Also, the number of plants that produced new cysts was a function of inoculum density and not age of eggs. Juveniles from eggs 1 year old or older were equally as infective as were those from eggs in newly developed cysts (4 months old).     

Chemical control of potato cyst-nematode in sandy clay soil

In sandy clay soil in Bedfordshire, potato cyst-nematode (Heterodera rostochiensis Woll.) was controlled and yields of Majestic potatoes greatly increased when i-2g aldicarb, 4-0 g fensulphothion or 10-3 g diazinon, disulphoton, ‘Isolan’ (i-isopropyl-3-methyl-5-pyrazolyl dimethylcarba-mate) or thionazin per m² were incorporated in the top soil before potatoes were planted. Diethyl phosphorothioates controlled H. rostochiensis better than dimethyl phosphates. One hundred and eleven g methyl bromide, 47-6 g carbon disulphide or 45-2 g D-D per m² applied to the soil and covered with polyethylene sheeting greatly increased the yield of potatoes, but also increased the number of nematodes in the soil. Estimates of the number of larvae able to invade potato roots in treated soil after harvest and of cysts, total eggs or live eggs selected the same range of treatments as effective in controlling H. rostochiensis.     

Emergence of juvenile potato cyst-nematodes Globodera rostochiensis and G. pallida and the control of G. pallida

Speed of emergence of juveniles from cysts in potato root diffusate (PRD) in vitro differed between Globodera rostochiensis and G. pallida and between populations within each species. Early emergence in vitro was slower in most populations of G. pallida than in most populations of G. rostochiensis. Fewer G. rostochiensis juveniles emerged from 4 or 6 month old than from 4 yr old cysts. More G. rostochiensis emerged in solutions of sodium metavanadate at concentrations of 10^-2 and 10^-3 M than in PRD and as many G. pallida emerged in the same solutions as in PRD. In plots of bare fallowed sandy loam, emergence of G. pallida was stimulated by 10^--³ M sodium metavanadate. The emergence of two populations of C. pallida in PRD was stimulated by the addition of benomyl at 0.1 ppm (3.4 × 10^--⁷ m). In microplots, cv. Cara potatoes grown for 8 wk decreased four populations of G. pallida by up to 93%. During a 4 wk period in PRD, more than 20 juveniles per gravid female emerged from five of 25 populations of G. pallida. In root observation boxes in which cv. Désirée was grown, oxamyl applied to the top 15 cm of a peaty loam soil greatly increased G. pallida in soil 1545 cm deep. In another peaty loam, but not in a sandy loam, the same treatment appeared to increase the nematode in soil 15–30 cm deep. Oxamyl incorporated in the uninfested top 15 cm of all three soils largely prevented nematode increase from juveniles migrating upwards from untreated heavily infested soil 15–30 cm deep. These experiments suggest that inadequate control of G. pallida increase on susceptible potatoes by an oximecarbamate nematicide of short persistence, such as oxamyl, is primarily due to the slow rate of juvenile emergence in most populations of G. pallida, with a second generation and the upward migration of juveniles from deeper untreated soil later in the growing season as potential contributory factors.     

Observations on periodicity of hatching of eggs of the potato cyst nematode, Heterodera rostochiensis Woll.

Soil containing new-generation cysts of Heterodera rostochiensis was taken from the field at monthly intervals during late summer and autumn and kept in various conditions for up to a year. The number of eggs that hatched in the stored cysts was compared each month with the number that hatched in cysts taken directly from the field. Eggs did not hatch readily when stimulated during the late autumn and early winter, although more did so in cysts taken from the field before August than after. A few more eggs hatched in cysts stored in air-dried soil than in cysts stored in moist soil. Some cysts were kept at 15 or 20 °C continuously and others at 5, 15 or 30 °C for 6 weeks followed by 20 °C continuously. Storage at 30 °C caused eggs to hatch sooner, but otherwise the temperature of storage had little effect on hatch at any time of the year. Warmth also increased the hatch of H. cruciferae sooner, and some synthetic hatching agents did so with both of these species. When freed from new cysts, more eggs of H. rostochiensis hatched than in intact cysts and hatch was further increased when the fragments of tanned cyst-wall were left with the freed eggs. Puncturing the cyst-wall of new brown cysts had little effect on the hatch in potato root diffusate. Like eggs in new cysts, those in 1-year-old cysts stored out of doors ceased to hatch during the autumn and winter. The term ‘dormancy’ is inadequate to describe the inability of eggs of H. rostochiensis and other Heterodera spp. to hatch in the appropriate stimulant and the term ‘facultative diapause’, as applied to insects, better fits the phenomenon.     

Potato cyst nematodes in England and Wales - occurrence and distribution

Potato cyst nematodes (PCN) have been known to occur in the UK for nearly a hundred years. They are the most problematic pests of potatoes and can cause severe yield losses. Previous work has shown the two species, Globodera rostochiensis and G pallida, to be distributed throughout the UK. This paper reports the results of the first structured and statistically unbiased survey undertaken to assess their occurrence and distribution in the potato growing land of England and Wales. The survey showed that PCN were present in 64% of sites sampled. Of the populations found, 67% were G pallida, 8% were G rostochiensis and 25% contained both species. The results show an increase in the incidence of PCN since previous studies were completed and confirm the perceived shift towards G pallida as the predominant species. Of the infestations found, 62% had a population density of less than 10 eggs g^?1 soil.     

Effect of Initial Nematode Density on Managing Globodera rostochiensis with Resistant Cultivars and Nonhosts

Cropping systems in which resistant potato cultivars were grown at different frequencies in rotation with susceptible cultivars and a nonhost (oats) were evaluated at four initial nematode population densities (Pi) for their ability to maintain Globodera rostochiensis at a target level of <0.2 egg/cm³ of soil. At a Pi of 0.1 to 1 egg/cm³ of soil, cropping systems with 2 successive years of a resistant cultivar every 3 years of potato production reduced and maintained G. rostochiensis at <0.2 egg/cm³ of soil. At a Pi of 1 to 4 eggs/cm³ of soil, 2 successive years of a resistant cultivar followed by 1 year of oats for every 4 years of production were necessary to reduce and maintain G. rostochiensis populations at <0.2 egg/cm³ of soil. At a Pi greater than 4 eggs/cm³ of soil, 2 successive years of a resistant cultivar plus 1 year of oats reduced G. rostochiensis densities to <0.2 egg/cm³ of soil, but the population increased above that density after cropping 1 year to a susceptible cultivar. The numbers of cysts and eggs per cyst in the final population (Pf) of G. rostochiensis were influenced by initial density and the frequency of growing a susceptible cultivar in a cropping system. The lowest number of cysts and eggs per cyst in the final G. rostochiensis population occurred with a cropping system consisting of 2 successive years of a resistant cultivar followed by oats with a susceptible cultivar grown the fourth year of production.     

Influence of nematicide, resistant and susceptible potato cultivars and bare fallow on the population dynamics of Globodera rostochiensis Woll. Rol under field conditions in Spain

The susceptible potato cultivar Désirée and the resistant cv. Diamant were cultivated on untreated and nematicide-treated plots on two fields in northern Spain infested with Globodera rostochiensis Rol. Initial and final infestations of cysts and viable eggs were assessed. Multiplication rates differentiated more accurately the effects of the different treatments than final number of cysts and eggs, due to the elimination of some of the errors associated with variability of the initial infestation. Many new cysts were observed on all plots where susceptible potatoes had been grown, whether they had been treated with nematicide or not, although significantly fewer cysts were actually found on the nematicide-treated plots. With the resistant cultivar no significant effects of the nematicide were detected even though there was a noticeable reduction of viable cyst contents over and above the effect of the resistant cultivar.     

The resistance of six potato cultivars to English populations of potato cyst-nematodes, Globodera pallida and G. rostochiensis

Six cultivars of potato (Santé, Morag, Paladin, Glenna and Fingal bred for resistance to both potato cyst-nematodes (Globodera rostochiensis and G. pallida) and Valiant bred for resistance to G. pallida alone) were exposed to 28 English populations of G. pallida and eight English populations of G. rostochiensis in pots. Susceptible cv. Désirée potatoes served as controls for all 36 populations. Inoculum (Pi) was 12000 eggs in cysts per 400ml pot of soil. Average increase of G. rostochiensis (Pf/Pi) on cv. Désirée was 23.5 but on cvs Sante, Glenna and Fingal it was < 1.0 and on cv. Morag it was 2.2. In contrast, cvs Paladin and Valiant were susceptible (average Pf/Pi = 17.4 and 26.5, respectively). Against G. pallida populations, average Pf/Pi for cv. Désirée was 21.7; on cvs Paladin, Santé and Glenna it was 2.9, 2.6 and 2.4, respectively; cvs Morag and Fingal were less resistant (7.4 and 5.6, respectively) and cv. Valiant was quite susceptible (11.0). Resistance to the different populations of G. pallida and G. rostochiensis varied but for the most resistant cultivars (Santé, Glenna and Paladin) the variation was usually small. The value of the six resistant cultivars studied to the integrated control of potato cyst-nematodes in England and the genetic diversity of the nematode populations to which they were exposed are discussed.     

Observations on the distribution of potato cyst-nematodes, Globodera rostochiensis and G. pallida on two fenland potato farms

The distribution of potato cyst-nematodes, Globodera rostochiensis and G. pallida was surveyed in two widely separated fenland potato farms in Eastern England. Evidence was obtained of the suppression of G. rostochiensis and increase of G. pallida populations when Maris Piper and other potatoes with the same gene (H₁) for resistance to G. rostochiensis are grown. Numbers of G. rostochiensis and/or G. pallida in the soil could not be related directly to recent potato cropping histories of the fields. Identification of the two species of Globodera by the presence and colour of females on the roots of Désirée, Maris Piper, Cromwell (A27/20) and A25/11 potatoes were confirmed by agarose gel isoelectric focussing of general proteins. Cromwell exhibited little or no resistance to G. pallida at Woodwalton. A25/11 was more resistant to this species at Woodwalton but was susceptible to G. rostochiensis. The results of these surveys emphasise the need for carefully planned and integrated control programmes based on the use of resistant cultivars of potato, crop rotations and appropriate nematicide use to combat the growing problem of G. pallida, especially in organic soils.     

Observations on the control of potato cyst-nematodes, Globodera rostochiensis and G. pallida in 35 English potato soils in pots by oxamyl and resistant potatoes

The increase of 35 English field populations of potato cyst-nematodes (Globodera rostochiensis and/or G. pallida) was measured on Désirée, Maris Piper, Caxton (A25/11), Cromwell (A27/20) and clone 11233 ab 22 in pots of sandy, silty or peaty loam soil. Désirée was susceptible to all populations tested and, as in field soils, the final population (Pf) was inversely related to the initial population of potato cyst-nematode eggs (Pi) in the soil. Maris Piper and Cromwell were resistant to all G. rostochiensis populations, with one possible exception. Maris Piper was susceptible to all G. pallida populations. Caxton was susceptible to some and fairly resistant to other populations of G. rostochiensis, indicating the existence either of two biotypes within the one pathotype (Rol) as yet encountered in Britain, or the existence of an additional pathotype. Caxton and Cromwell were fairly resistant to G. pallida. Clone 11233 ab 22 was only moderately resistant to both species. Resistance to potato cyst-nematode increase varied considerably, especially in Caxton (to G. rostochiensis) and in 11233 ab 22 (to both species). Oxamyl greatly reduced the increase of G. rostochiensis populations on Désirée potatoes, with the notable exception of one population but it generally had much less effect on G. pallida populations, regardless of soil type. The difference in effect on the two species may be due to a longer period of hatching in G. pallida than in G. rostochiensis and also perhaps to a second generation in G. pallida.     

Evaluation of Pochonia chlamydosporia var. chlamydosporia as a control agent of Meloidogyne javanica on pistachio

The potential of isolates of Pochonia chlamydosporia var. chlamydosporia as biocontrol agents for root-knot nematodes was investigated in vitro and on pistachio plants. On potato dextrose agar, growth of all isolates started at temperatures above 10°C, reached maximum between 25 and 28°C and slowed down at 33°C. On water agar, all isolates parasitized more than 85% of the eggs of Meloidogyne javanica at 18°C after 3 weeks. Filtrates of isolates grown on malt extract broth did not cause more than 5% mortality on second-stage juveniles of M. javanica after 48 h of incubation. A single application of 10×10³ chlamydospores (produced on sand–barley medium) g^–1 soil, was applied to unsterilised soil planted with pistachio cv. Kalehghochi, and plants were inoculated with 3000 nematode eggs. After 120 days in the glasshouse, nematode multiplication and damage were measured. Ability of fungus isolates to survive in the soil and to grow on roots were estimated by counting colony forming units (cfu) on semi-selective medium. Fungal abundance in soil increased nearly 3-fold and 10×10³ and 20×10³ cfu g^–1 root of pistachio were estimated in pots treated with isolates 40 and 50, respectively. Strain 50 was more abundant in soil and on the roots, infected more eggs (40%) on the roots and controlled 56% of total population of M. javanica on pistachio roots, whereas isolate 40 parasitized 15% of the eggs on the roots and controlled ca. 36% of the final nematode population.     

Effect of coexistence of Penicillium frequentans (westling) with Globodera rostochiensis (Woll.) behrens on potato

The aim of two‐year‐long pot experiments was to investigate the influence of P. frequentans on the growth of over‐ground parts, the intensity of assimilation and transpiration of plants, as well as ths influence on the yield of potato bulbs. It was determined how the above fungus influenced the populaüon of G rostochiensis, the influence being characterized by the density change of cysts, eggs, and larvae in the soil. Experiments in vitro allowed to determine the wholesomeness of cysts, eggs, and larvae (J2) that were in direct contact with the mycelium ofP. frequentans.

It was stated that presence of P. frequentans intensified the development of plants and relevantly stimulated their growth, especially in the initial vegetation phase, as compared with the remaining combinations (Fig. 1). Positive effect of P. frequentans on the growth of potato yield was proved, in comparison with the control, and by co‐occurrence of the fungus with G. rostochiensis, also in comparison to the combination with nematodes only (Fig. 2).

Pot experiments confirmed the antagonistic effect of P. frequentans on the population of G. rostochiensis. Presence of P. frequentans in the ground caused namely a relevant diminution of density of cysts, eggs and larvae (Tab. II), as well as morphological changes by females, which was connected with size reduction of the cysts (Tab. III). Experiments in vitro confirmed the destructive effect of P. frequentans on the cysts of G. rostochiensis (Tab. IV).     

Differential control of potato cyst-nematodes, Globodera rostochiensis and G. pallida by oxamyl and the yields of resistant and susceptible potatoes in treated and untreated soils

In sandy loam infested with Globodera rostochiensis (2–95 eggs g^-1 soil) the yield of Desiree potatoes was decreased by 8·2 t ha^-1 for every increment of 20 eggs g^-1 soil. Oxamyl incorporated in the seedbed at 5 kg ha^-1 before planting prevented significant loss of yield and damage to the tubers and minimised nematode increase. Cara and Maris Piper potatoes, which were resistant and tolerant to G. rostochiensis usually responded less to oxamyl than did susceptible cultivars. In a range of cultivars, yield responses to oxamyl treatment of soil infested with G. rostochiensis often differed from those in soil infested with G. pallida. In field experiments, oxamyl controlled G. pallida less than G. rostochiensis. In pots, such differential control of the two species by oxamyl was not observed.     

The behaviour of populations of potato cyst eelworm Heterodera rostochiensis Woll. Towards resistant potato varieties derived from Solarium tuberosum ssp. andigena Juz & Buk

Many populations of Heterodera rostochiensis mostly from the main potato growing areas of England and Wales, were tested with eelworm-resistant potato varieties (andigena hybrids). Except in the Eastern Region, where resistant varieties were planted alongside commercial varieties in infested fields, tests were done in pots inoculated with a standard number of cysts extracted from a single soil sample from each field. The tests showed that England and Wales could be divided into areas according to the percentage of cysts(< 10%, 11–70%,> 70%) produced on the resistant compared with a commercial non-resistant variety. On the peat soils of the East Anglian fens and in Bedfordshire, Essex and Kent (area A) most populations produce few cysts on resistant varieties. In much of the East Midlands and Yorkshire (area D), populations produce many cysts on resistant varieties which behave much as ordinary susceptible potatoes. Populations in the rest of England and Wales (areas B, C) vary and in many districts every field must be tested separately. If the pathotypes occurring in Britain had separate origins in South America, the present distribution in England and Wales is probably due to chance introductions dispersed with seed and following the patterns of trade in seed potatoes. As all commercial varieties, before the release of eelworm-resistant ones, were about equally susceptible to the different pathotypes, the varieties themselves probably played little part in determining the present distribution of pathotypes.     

On cyst colour changes, bionomics and distribution of potato cyst-eelworm (Heterodera rostochiensis Woll.) pathotypes in the East Midlands

Pot tests and field trials in 1966 confirmed earlier observations that pathotype A potato cyst-eelworm (Heterodera rostochiensis Woll.) showed marked colour differences from pathotypes B and C during development on the roots of susceptible potatoes. In hatching tests started in July, newly formed brown cysts of pathotype A released four times as many larvae as those of pathotypes B and C, without entering an immediate diapause; the latter produced larvae after a rest period of 18–21 days. Subsequent second-generation cyst production in glass-tube culture was greater from pathotype A. Field observations suggested that all pathotypes mature at about the same time and give rise to only one flush of cysts on both early and maincrop potatoes in the growing season. Cyst colour surveys in commercial crops, and pot and field trials using resistant potato selections, confirmed that pathotypes B and C are both dominant and widespread in the East Midlands.     

The Relationship between Temperature and Development in Globodera ellingtonae

A new cyst nematode species, Globodera ellingtonae, was recently described from populations in Oregon and Idaho. This nematode has been shown to reproduce on potato. Because of this nematode’s close relationship to the potato cyst nematodes, G. rostochiensis and G. pallida, an understanding of the risk of its potential spread, including prediction of potential geographical distribution, is required. To determine the development of G. ellingtonae under different temperatures, we conducted growth chamber experiments over a range of temperatures (10.0°C to 26.5°C) and tracked length of time to various developmental stages, including adult females bearing the next generation of eggs. Both the time to peak population densities of G. ellingtonae life stages and their duration in roots generally increased with decreasing temperature. Regression of growth rate to second-stage (J2) and third-stage (J3) juveniles on temperature yielded different base temperatures: 6.3°C and 4.4°C for J2 and J3, respectively. Setting a base temperature of 6°C allowed calculation of the degree-days (DD6) over which different life stages occurred. The largest population densities of J2 were found in roots between 50 and 200 DD6. Population densities of J3 peaked between 200 and 300 DD6. Adult males were detected in soil starting at 300 to 400 DD6 and remained detectable for approximately 500 DD6. By 784 to 884 DD6, half of the eggs in adult females contained vermiform juveniles. Given the similarity in temperature ranges for successful development between G. ellingtonae and G. rostochiensis, G. ellingtonae populations likely could survive in the same geographic range in which G. rostochiensis now occurs.     

Climate change is predicted to alter the current pest status of Globodera pallida and G. rostochiensis in the United Kingdom

The potato cyst nematodes Globodera pallida and G. rostochiensis are economically important plant pathogens causing losses to UK potato harvests estimated at £50 m/ year. Implications of climate change on their future pest status have not been fully considered. Here, we report growth of female G. pallida and G. rostochiensis over the range 15 to 25°C. Females per plant and their fecundity declined progressively with temperatures above 17.5°C for G. pallida, whilst females per plant were optimal between 17.5 and 22.5°C for G. rostochiensis. Relative reproductive success with temperature was confirmed on two potato cultivars infected with either species at 15, 22.5 and 25°C. The reduced reproductive success of G. pallida at 22.5°C relative to 15°C was also recorded for a further seven host cultivars studied. The differences in optimal temperatures for reproductive success may relate to known differences in the altitude of their regions of origin in the Andes. Exposure of G. pallida to a diurnal temperature stress for one week during female growth significantly suppressed subsequent growth for one week at 17.5°C but had no effect on G. rostochiensis. However, after two weeks of recovery, female size was not significantly different from that for the control treatment. Future soil temperatures were simulated for medium‐ and high‐emission scenarios and combined with nematode growth data to project future implications of climate change for the two species. Increased soil temperatures associated with climate change may reduce the pest status of G. pallida but benefit G. rostochiensis especially in the southern United Kingdom. We conclude that plant breeders may be able to exploit the thermal limits of G. pallida by developing potato cultivars able to grow under future warm summer conditions. Existing widely deployed resistance to G. rostochiensis is an important characteristic to retain for new potato cultivars.     

Morphological variability of potato cyst nematodes (Globodera spp.) in the Canary Islands

Thirty populations of potato cyst nematode (Globodera spp.) from the Island of Tenerife and two populations from the UK were assessed for several morphometric and non-morphometric characters thought to discriminate between the species G. rostochiensis and G. pallida. Also 200 cysts from each population were analysed by isoelectric focusing of soluble proteins. Correlation analysis, analysis of variance and principal component analysis were used to investigate relationships between the morphometric characters, how the relationships varied between species and between populations, and which characters were most useful for discriminating between species. The two species differed significantly for each of the four morphometric characters: stylet length, fenestra length, anus-fenestra distance and the number of ridges. The stylet length and fenestra length also showed differences between populations of G. rostochiensis while stylet length and number of ridges showed differences between populations of C. pallida. In general, populations of G. pallida showed greater variation than populations of C. rostochiensis. Principal component analysis of the population means indicated that over 73% of the variation in the characters could be explained by the contrast of stylet and fenestra lengths against the anus-fenestra distance and number of ridges. A plot of the first two principal components separated the two species. Stepwise discriminant analysis provided a linear combination of these four variables which discriminated between the species. Stylet length was found to be the most useful characteristic for distinguishing the species whilst anus-fenestra distance was the least useful.