Arthropod pests of currant and gooseberry crops in the U.K.: their biology,management and future prospects

• 1 Approximately 10–12 species of Ribes plants are cultivated for fruit production, mainly blackcurrants, red‐ and whitecurrants and gooseberries. These crops are increasingly recognized as rich sources of vitamin C and anthocyanins, with production rising by 24% in Europe subsequent to 1998. To date, research into insect pests of Ribes has been fragmented, with little appreciation of how changes in climate and agronomic practices affect biology.
• 2 We review 12 key pests of currant and gooseberry crops in Northern Europe, with specific emphasis on their biology and current management options. These are blackcurrant leaf curling midge Dasineura tetensi, blackcurrant sawfly Nematus olfaciens, common gooseberry sawfly Nematus ribesii, European permanent currant aphid Aphis schneideri, redcurrant blister aphid Cryptomyzus ribis, currant–sowthistle aphid Hyperomyzus lactucae, European gooseberry aphid Aphis grossulariae, woolly vine scale Pulvinaria vitis, common green capsid Lygocoris pabulinus, winter moth Operophtera brumata, clear wing moth Synanthedon tipuliformis and blackcurrant gall mite Cecidophyopsis ribis.
• 3 It is anticipated that global climate change could lead to increases in the incidence of some aphids through increased overwintering survival and longer seasonal activity. Moreover, changes in management practices such as increased cropping densities (from 5400 ha^?1 to 8700 ha^?1) and machine harvesting could lead to pest outbreaks through optimal microhabitats and increased susceptibility to pest colonization.
• 4 Future management options are considered, focusing on integrated pest management approaches, including behaviour‐manipulating semiochemicals, predictive models, biocontrol and improved plant resistance through breeding.

     

Ultrastructure of the black currant gall mite, Cecidophyopsis ribis (Acari: Eriophyidae), the vector of the agent of reversion disease

Electron microscopy of ultrathin serial sections was used to determine the structure and anatomy of the eriophyid gall mite, Cecidophyopsis ribis, the vector of the agent of black currant reversion disease. The composite picture derived from these studies has determined the location of the food canal, and major internal organs of the mite. Detailed ultrastructural studies on the anterior of suitably orientated mites has also provided detailed information on the geometry and complex structure of three sets of stylets in the feeding apparatus. No evidence was found of structures resembling virus-like particles or of other described plant pathogens in the feeding apparatus and food canal of mites obtained from black currant plants affected with reversion disease. However, little or no food was apparently present in the food canal of most mites examined. This is the first detailed report of the anatomy and the ultrastructure of the mouthparts of this important plant pest and vector.     

Overwintering of Sphaerotheca mors-uvae on black currant and gooseberry

The ability of Sphaerotheca mors-uvae to perennate as cleistocarps, and as mycelium in buds was examined during the winters of 1965-6, 1966-7 and 1967-8 in relation to its two principal hosts, gooseberry and black currant. Cleistocarps on black currant leaves were examined from August 1965 to April 1966 and from July 1966 to March 1967. In 1965 cleistocarps were first observed on the leaves on 5 August; in 1966 on 11 July. These continued to develop through August and September and by October approximately 70% contained well-defined ascospores. The ascospore content remained generally at this level until February 1966 and November 1966; then the numbers of cleistocarps with ascospores fell and by April 1966 and March 1967 few such cleistocarps remained. From 21 March 1966 and 15 February 1967, but not otherwise, discharge of ascospores from the overwintered cleistocarps was readily obtained in laboratory tests. The viability and infectivity of the ascospores was demonstrated by allowing them to discharge on to leaf discs of black currant in the laboratory and also on to leaf discs and plants in the field. Sporulating colonies of S. mors-uvae developed within 8 days. Cleistocarps from shoots of black currant were examined from 4 August 1966 to 9 March 1967, and from 27 July 1967 to 1 January 1968. They developed in a similar manner to those on black currant leaves and by September in both 1966 and 1967 over 60% contained ascospores. This level was not maintained; the number of cleistocarps with ascospores fell gradually and by 8 December 1966 and 1 January 1968 few remained. Only in one laboratory test (21 November 1967) were ascospores discharged from a sample of these cleistocarps. Cleistocarps from shoots of gooseberry were examined from July 1966 to March 1967, and from August 1967 to January 1968. The pattern of ascospore development and subsequent decline in number of cleistocarps with ascospores was similar to that observed for black currant shoots. No discharge of ascospores could be demonstrated in laboratory tests. Evidence that S. mors-uvae perennates in buds of gooseberry was obtained by dissecting buds and by inducing buds on surface-sterilized shoots to burst under conditions which precluded chance infection. Field observations also suggested that bud infection occurred on gooseberry. Similar experiments failed to demonstrate the fungus in buds of black currant, and there was no indication of bud infection of this host in the field.     

Characteristics of development and reproduction in Typhlodromus pyri on Tetranychus urticae and Cecidophyopsis ribis. II. Progeny of overwintered females

The results of this study on the bionomic parameters in progeny of overwintered females of Typhlodromus pyri Scheuten under constant laboratory conditions (18°C, R.H. 75%. 18L:6D) are described. The predatory mites were fed overwintering forms of two prey species, the two-spotted spider mite. Tetranychus urticae Koch and the black currant gall mite. Cecidophyopsis ribis (Westwood). The results corroborate that T. pyri is able to complete its life-cycle and reproduce when it feeds exclusively on the black currant gall mite. Juvenile development of females feeding on T. urticae and on C. ribis was 19.4 and 20.9 days respectively, while in males it was 18.4 and 17.5 days. Mortality of juveniles feeding on T. urticae was higher (33.0%) compared with that of juveniles fed on C. ribis (10.7%). The highest mortality was noted in protonymphs fed on T. urticae (21.9%). The difference between the mean total fecundity of females fed on T. urticae (16.4 eggs) and on C. ribis (17.8 eggs) was not statistically significant. Mean duration of preoviposition, oviposition and postoviposition periods were 19.1, 25.0 and 14.5 days in females fed on T. urticae and 19.7. 50.2 and 5.0 in those fed on C. ribis.     

The life-history and epidemiology of American gooseberry mildew on black currants

It is shown that conidia of Sphaerotheca mors-uvae (Schw.) Berk, from gooseberry readily infect black currant; therefore it is unlikely that a new race of S. mors-uvae specifically pathogenic to black currants has recently appeared. However, the life-cycle on black currants differs from that on gooseberry. Incubation, infection and sporulation of the fungus have been examined under the optimum conditions of 18 °C and 100% relative humidity. The establishment of infections and sporulation was encouraged by a relatively low soil moisture content, temperatures above 15 °C, 60% relative humidity and good illumination-factors which promote vigorous plant growth. High phosphorus and high potassium nutrition also increased the susceptibility of black currants to infection.     

Biotypes of Dasineura tetensi, differing in ability to gall and develop on black currant genotypes

Variation in damage levels on certain black currant, Ribes nigrum L., genotypes, caused by the black currant leaf midge, Dasineura tetensi (Rübs.) (Diptera: Cecidomyiidae), has been observed in northern Sweden. I investigated whether this variation is due to variation in virulence among midges. From a field population of midges, I successfully selected for virulence and avirulence, respectively, on the resistant black currant genotype cultivar `Storklas' (called resistant genotype). The performance of avirulent and virulent midge larvae on two black currant genotypes were studied in experiments where first or second instar larvae were artificially transferred. There were no differences in larval survival and developmental rate between the two midge types when transferred to the susceptible currant genotype `7801–31' (called susceptible genotype). Larvae of the virulent strain established galls and developed on `Storklas' but development was initially slower there than on the susceptible currant genotype. Larvae of the avirulent strain suffered high mortality or remained in first instar on that same currant genotype when transferred alone, but developed readily if transferred together with virulent larvae. Larvae transferred in second instar to host plants susceptible to the larvae resumed feeding and developed further to maturity. Second instar larvae were also able to establish new galls even though these galls were not as well developed as those caused by first instar larvae. Black currant plantations in northern Sweden were surveyed and local midge populations were found to be composed of either avirulent, virulent or a mixture of both midge types. Virulent midges were not restricted to plantations where resistant currant genotypes were grown. I conclude that, at least, two biotypes of the midge exist, and that those two are distinguished by the ability to gall and survive on `Storklas'.     

Study of genetic variability of representatives of <Emphasis Type="Italic">Ribes</Emphasis> L. grown in Belarus

The study of genetic variability of Ribes L. representatives grown in Belarus using seven loci of microsatellite sequences showed that modern Belarusian varieties of black currant are characterized by high genetic variability and have a close genetic relationship with foreign selection varieties. The number of alleles in the studied loci varied from 5 to 11. The average number of unique genotypes among 65 samples was 43.1. The discrimination power of the markers varied from 0.67 to 0.95 and the mean value was 0.84. All markers have rather high diagnostic value and make it possible to identify black currant and gooseberry varieties at the molecular level and, therefore, can be recommended for DNA-identification of these cultures.     

Species identification of Cecidophyopsis mites (Acari: Eriophyidae) from different Ribes species and countries using molecular genetics

Cecidophyopsis mites were studied by PCR amplification of parts of their ribosomal DNA, followed by restriction enzyme analysis. Mite specimens on Ribes nigrum (black currant) from six countries gave the same digestion pattern, which was distinct from the pattern for mites found on R. rubrum from Poland and Finland and for R. grossularia from the USA. This suggests that each Ribes species is host to a different mite species: C. ribis, C. selachodon and C. grossulariae, respectively. Two other mite samples from R. alpinum and R. aureum were identical but were distinct from each of the other species.     

Evaluation of a modified encapsulation-dehydration procedure incorporating sucrose pretreatments for the cryopreservation of <Emphasis Type="Italic">Ribes</Emphasis> germplasm

Summary A modified encapsulation-dehydration cryopreservation protocol based on the replacement of cold acclimation with high-sucrose pretreatment was assessed for the long-term storage of Ribes germplasm. Four steps in the procedure were examined for eight genotypes: (1) pregrowth of shoot tips in sucrose-supplemented solid growth medium for 1 wk; (2) pretreatment of alginate-encapsulated shoot tips in sucrose-supplemented liquid culture medium for 21 h; (3) evaporative desiccation of encapsulated-dehydrated shoot tips; and (4) exposure to liquid nitrogen (LN). Differential responses were observed for black currant and gooseberry genotypes. Recovery of growing shoots was high (72–100%) at all four steps for the five black currants tested. Evaporative desiccation slightly decreased viability for some black currants and in some cases LN exposure reduced regrowth. In contrast, three gooseberry species had poor recovery from the initial sucrose culture step (32–67%), indicating sensitivity to osmotic stress, which predisposed these genotypes to poor survival after LN exposure (12–26%). The effectiveness of the modified protocol for conserving a wider range of Ribes genotypes was further ascertained by screening 22 genotypes derived from nine Ribes species. The procedure was successful for 18 of the 22 genotypes in the gene bank in Scotland. Screening genotype responses at the time of storage demonstrated regrowth ≥60% for 15 genotypes, and only four genotypes had regrowth of 0–28%. Additional genotypes were also added to the USDA cryopreserved Ribes collection.     

Host specificity ofAceria (Eriophyes) malherbe, [Acari: Eriophyidae], a biological control agent for the weed,Convolvulus arvensis [Convolvulaceae]

The host specificity of the gall mite,Aceria (Eriophyes) malherbe (Nalepa), from Greece was studied under quarantine conditions at Albany, California USA. Of the species, ecotypes, or strains tested, onlyConvolvulus andCalystegia spp. supported gall formation and mite reproduction. Although 2 of the native, North AmericanCalystegia species that served as laboratory hosts are threatened or endangered species,A. malherbe is considered safe for release in the USA as a biological control agent of the weed,Convolvulus arvensis (L.).      

Molecular ecology of some Cecidophyopsis mites (Acari: Eriophyidae) on Ribes species and evidence for their natural cross colonisation of blackcurrant (R. nigrum)

Ribosomal DNA from Cecidophyopsis mites from different Ribes species was amplified using the polymerase chain reaction and the products digested using restriction enzymes. After separating the DNA fragments on gels, it was possible to identify specimens of mites obtained from field samples by comparing the profiles of their DNA banding patterns with those of known Cecidophyopsis species. Using this analysis, a non-gall forming mite found infesting blackcurrant buds in New Zealand was identified as the gooseberry mite (C. grossulariae). On wild red currant (Ribes spicatum) from Finland showing two sizes of galled buds, the red currant gall mite (C. selachodon) was identified in the larger galls located at the tips of branches and a distinct mite in the smaller galls located on the lower parts of the branches. A mite with a DNA banding profile indistinguishable from this latter mite from R. spicatum was also identified in galled buds of blackcurrant genotypes growing in Finland, including those containing the blackcurrant gall mite (C. n'ftw)-resistance genes P or Ce. The DNA banding profile of this mite resembled most closely that of C. ribis , but was distinct from it. The occurrence of C. grossulariae and this distinct Cecidophyopsis mite on blackcurrant has implications for the genetic control of Cecidophyopsis mites and possibly for the spread of the reversion disease agent in this crop.     

Galling and reversion disease incidence in a range of blackcurrant genotypes, differing in resistance to the blackcurrant gall mite (Cecidophyopsis ribis) and blackcurrant reversion disease

An assessment was made of the response of 10 blackcurrant genotypes, differing in resistance to the agent of blackcurrant reversion disease (BRD) and to its gall mite vector, in field trials in Scotland and Finland over 5 yr. At each location, the 10 genotypes were planted in plots containing infector plants with high inoculum levels of the two organisms. In Scotland, the infector plants contained large numbers of gall mites (Cecidophyopsis ribis) and were infected with the European (E) form of BRD; in Finland, infector plants contained a different species of gall mite (C. spicata) and the severe Russian form (R) of BRD. As expected, at both sites, almost all plants of cvs Ben Alder, Ben Lomond, Ben Tirran, Ojebyn and an SCRI selection F4/1/66, which are susceptible to gall mite and BRD, became infested with each of these organisms. However, in Scotland but not in Finland, 58% of cv. Ojebyn plants were affected by BRD. The cv. Foxendown, which contains gene Ce that confers apparent immunity to C. ribis, was free from galls and failed to develop distinctive BRD symptoms at both sites. The cvs Rus and Neosypajuscajaija, which contain gene P which is reported to confer resistance to C. ribis, were infested more slowly by mites than the mite-susceptible genotypes and showed a smaller number of galls per plant. Also, they were infected with BRD more slowly than some mite-susceptible genotypes although by the end of the experiment, most plants were affected by BRD. All plants of cvs Golubka and Ben Gairn, which are resistant to the agent of BRD, remained free from distinct BRD symptoms at both sites despite the fact that plants contained galls. These data indicate the superiority of gene Ce over gene P for resistance to gall mites with the added benefit that the virtual immunity to gall mites provided by gene Ce provides a high level of protection against infection with BRD. The relative merits of these different forms of resistance to gall mites and BRD in blackcurrant are discussed in relation to present control methods for these two organisms and in the light of recent findings of different species of eriophyid mites on Ribes species.     

Field experiments on the spread of black currant reversion virus and its gall mite vector (Phytoptus ribis Nal.)

In two experiments the spread of reversion virus from a row of systemi-cally infected black currant bushes heavily infested by the gall mite vector (Phytoptus ribis Nal.) was predominantly in the direction of the winds prevailing during the dispersal period. On each side of the sources there was a curvilinear decrease of galled buds and of virus infection as distance increased. In another experiment a central source of mites and virus was surrounded by concentric hexagons comprising alternate rows of healthy and virus-infected bushes. At leaf-fall, galls were forty times more numerous on virus-infected than on healthy bushes; plants in the sector downwind developed the most galls and those upwind the least. On both healthy and virus-infected bushes in each sector, the incidence of galls decreased with increasing distance from the source. The gradients of infestation were steeper on healthy than on virus-infected bushes, especially in sectors upwind from the source. In some sectors the infestation gradients were distorted because many of the virus-infected bushes were so heavily infested that most of the buds became galled. The spread of virus to initially healthy plants decreased from 100 to 75% near the source, to zero at the periphery. More bushes became infected downwind from the source than upwind. In each experiment more bushes developed galls than later produced symptoms of virus infection, the incidence of which was positively correlated with the number of galls recorded the previous winter.     

The development of a PCR-based marker linked to resistance to the blackcurrant gall mite (Cecidophyopsis ribis Acari: Eriophyidae)

Gall mite (Cecidophyopsis ribis) is the most serious pest of blackcurrant (Ribes nigrum L.), causing the damaging condition known as 'big bud' and also transmitting blackcurrant reversion virus (BRV) within and between plantations. The identification of resistant germplasm is at present a time-consuming and expensive process, dependent on field infestation plots. Resistance based on gene Ce introgressed from gooseberry has been used in UK breeding programmes for blackcurrant. Using a bulked segregant analysis, 90 AFLP primer combinations were screened and a linkage map constructed around the resistance locus controlled by Ce. Sixteen of the primer combinations produced a fragment in the resistant bulked progeny and the gall mite-resistant parent, but not in the susceptible bulked progeny and parent; subsequent testing on individual progeny identified an AFLP fragment closely linked to gall mite resistance. This fragment, designated E41M88-280, was converted to a PCR-based marker based on sequence-specific primers, amplifying only in resistant individuals. Validation of this marker across a range of susceptible and resistant blackcurrant germplasm with different genetic backgrounds confirmed its reliability in the identification of mite-resistant germplasm containing gene Ce. The conversion of an AFLP fragment to a sequence-based PCR marker simplifies its application and therefore increases its utility for selection of mite-resistant germplasm in high-throughput breeding programmes for blackcurrant.     

Shoot doubling time: A quantitative parameter for characterizing shoot cultures in vitro

Shoot doubling time is proposed as a suitable parameter for characterizing in vitro propagation rates in shoot cultures. Doubling times were estimated for cultures of black currant and apple; for black currant, doubling times ranging from 14 to 115 days were obtained, depending on the concentration of benzyladenine in the culture medium. These doubling times, which were constant for each culture, were maintained for periods of up to 76 days and could apparently be sustained indefinitely. For one subculture period only, a shoot doubling time as short as 5.6 days was obtained for black currant at high cytokinin concentration (3 × 10⁻⁵ M), but this rate could not be sustained. Shoot doubling time is a convenient parameter for use in optimizing proliferation rates in shoot cultures; its use may also facilitate investigations into the mechanisms of processes underlying shoot proliferation in vitro.     

The gall miteAceria cladophthirus. I. Life-cycle,survival outside the gall and symptoms' expression on susceptible or resistantSolanum dulcamara plants

The gall miteAceria cladophthirus (Nalepa) is able to survice outside its gall on detached leaves ofSolanum dulcamara L. kept under non-aseptic in-vitro conditions. The survival rate of the females on susceptible leaves is about 90% after 1 day and 85% for the following days. In contrast, on resistant leaves, less than 40$ survive after 1 day while necrotic local lesions develop and later the mortality increases severely. However, the mite only completes its life-cycle on susceptible leaves. The life-cycle forA. cladophthirus takes about 12 days: six days for egg incubation and six days for two instars growth. Its life-history is simple, without alternating females specialised for hibernation; arrhenotokous parthenogenesis occurs in experimental conditions. Eggs do not play any role in gall formation. Immature stages induce gall symptoms but are less efficient than females. Mite feeding only induces complete gall symptoms on the less differentiated leaves of susceptible shoots. On susceptible detached leaves, gall symptoms are similar but weaker and their intensity decreases with increasing leaf age; fully expanded leaves remain free of symptoms.On resistant plants, mite feeding induces a hypersensitive response: necrotic local lesions, about 350 m in diameter, appear both on shoots and on detached leaves. However, young leaves develop smaller lesions than old ones. Females induce larger lesions than first larvae. Once necrosis formation is initiated, it proceeds to completion regardless of the duration of mite feeding.     

Gall mite Fragariocoptes setiger (Eriophyoidea) changes leaf developmental program and regulates gene expression in the leaf tissues of Fragaria viridis (Rosaceae)

The interaction of plants with certain types of parasites leads to the formation of galls, organised structures that create the habitat of the parasite, caused by an abnormal proliferation of host plant's cells under the influence of growth regulators, secreted by the parasite, or by the plant itself under the influence of the parasite. Arthropods, mites in particular, are the largest group of gall‐inducing phytoparasites, but the mechanisms of their interaction with plants remain virtually unexplored. The interaction of the gall‐inducing eriophyoid mite Fragariocoptes setiger with Fragaria viridis plants was used as a model gall–mite system where data were obtained on the changes in the histological structure of F. viridis leaf blades under the influence of the mites as well as F. viridis gene expression during gall formation. For histological purposes, gall formation was split into four stages with each corresponding to the age of the gall as well as to specific changes that occur during that period. A dramatic change of adaxial–abaxial polarity of the lamina throughout the four stages was observed. Moreover, qRT‐PCR analysis of F. viridis gene expression in the developing gall revealed changes in the expression levels of certain meristem‐specific genes, as well as the genes that determine adaxial–abaxial polarity and signalling of phytohormones.     

Breeding for resistance to American gooseberry mildew, Sphaerotheca mors-uvae, in the gooseberry (Ribes grossularia)

Strong resistance to American gooseberry mildew (Sphaerotheca mors-uvae) occurred in eight out of ten F₁ progenies from crosses of resistant North American Eugrossularia species with European gooseberry cultivars or seedlings. Bimodal segregations in four of these F₁'s and in one F₁ derived from the wild European Ribes grossularia uva-crispa suggested that each donor carried a major dominant resistance gene. Such a gene, Sph₁ was identified in a first backcross from R. oxyacanthoides. Accessions of R. oxyacanthoides, R. leptanthum and R. watsonianum proved the most promising donors of resistance to mildew and leaf spot (Pseudopeziza ribis).     

The life history of a gall‐inducing mite: summer phenology,predation and influence of gall morphology in a sugar maple canopy

• 1 Eriophyoid mites are among the most ubiquitous gall‐inducing arthropods, and are adapted species‐specifically to a broad diversity of plants, although their life histories remain poorly studied outside agricultural systems.
• 2 We examined the seasonal phenology of a leaf‐galling eriophyid mite, the maple spindle gall mite Vasates aceriscrumena (MSGM), in naturally occurring stands of sugar maple Acer saccharum in south‐central Ontario in 2007 and 2008.
• 3 Galls were first induced in spring (mid‐May) and were devoid of mites by late August. In the study region, MSGM appears to have at least two generations, with overwintering, deutogyne females that initiate galls in spring (mid‐May) after leaf flush, giving rise to a generation of protogyne (primary) females and a few morphologically similar males (<1 for every 10 females) and, subsequently, to a new generation of deutogyne females in mid‐July to early August. In July, some galls can be highly crowded, with 50–200 individuals per gall.
• 4 In addition, a tarsonemid mite, Tarsonemus acerbilis, was found in approximately 40% of MSGM galls examined. As much as 95.4% of galls in 2007 and 97.4% in 2008 that contained tarsonemid larvae did not contain MSGM eggs (by contrast, only 2.3% of tarsonemid‐free galls contained no MSGM eggs), suggesting that these juveniles feed, at least opportunistically, on MSGM eggs.
• 5 Gall ostiole morphology appeared to influence both MSGM and Tarsonemus densities within galls, with ‘open’ ostioles (versus ‘closed’) being much more susceptible to invasion by the tarsonemid. The latter is likely to be an important regulator of MSGM populations. We hypothesize that the two ostiole types are the result of selection pressures on the gall inducer, favouring closed gall entrances for increased protection, and possibly also on the host tree, favouring open galls to increase predator access.

     

Spatial Distribution of Galls Caused by <Emphasis Type="Italic">Aculus tetanothrix</Emphasis> (Acari: Eriophyoidea) on Arctic Willows

The distribution of galls caused by Aculus tetanothrix (Acari: Eriophyoidea) on three Salix species was studied. The factors influencing this distribution were analysed, i.e. willow species, study area and shoot length. Spatial pattern of gall distribution within the shoot was also examined. The study was conducted in Russia, Kola Peninsula. Densities of galls caused by A. tetanothrix differed significantly among willow species. Considerably higher gall density was recorded in the White Sea coast than in the Khibiny Mountains. This may be explained by the influence of a milder maritime climate that favors mite occurrence compared to a harsh and variable mountain climate that limits mite abundance. There was no relationship between the gall density and the shoot length. The highest density of galls was recorded on the inner offshoots; within the offshoot, there was a maximum density on the fifth leaf. This pattern was repeatable for all shoots studied, independent of the study area, willow species and length of shoots, suggesting the optimal conditions for A. tetanothrix exist on leaves in the middle part of a shoot. This distribution pattern may be an effect of the trade-off between the costs and benefits resulting from leaf quality and mite movement along the shoot. This hypothesis, however, needs to be tested experimentally.