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3.2.6 Currants and berries
Eriophyoid Mites - Their Biology, Natural Enemies and Control
583
E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors) 9 1996Elsevier Science B.V.All rights reserved.
3.2.6 Currants and Berries E. DE LILLO and C. DUSO
Eriophyoids are of economic importance in cultures of various small fruits (e.g., black and red currants, blueberry, blackberry). In this chapter their biology, injuriousness, natural enemies and pest management are discussed.
ERIOPHYOIDS
OF CURRANTS
Until now 18 species of eriophyoids have been found on Ribes spp., the majority on black currant, R. nigrum L. (Amrine and Stasny, 1994; Amrine et al., 1994). Recently, Amrine et al. (1994) reviewed closely-related species in the genus Cecidophyopsis occurring on Ribes spp. showing significant morphological differences. Moreover, they reviewed their geographical distribution, biology and host relationships, revealing a high specificity for individual species of Ribes confirmed by molecular evidence of the mite ribosomal DNA (Fenton et al., 1995). Among these species, C. ribis (Westwood) appears to be the most noxious, as it causes direct damage to the buds and indirect damage to the plant.
Cecidophyopsi$ ribis This species occurs mainly in Europe and is commonly called "black currant bud mite" or "big bud mite". It was previously known under the generic names P h y t o p t u s (Nalepa, 1893), Eriophyes (Nalepa, 1898), Cecidophyes (Keifer, 1946) and finally Cecidophyopsis (Massee, 1961). Bionomics The biology of the big bud mite has been studied by Massee (1928), Collingwood and Brock (1959), Smith (1959, 1961) and Thresh (1967) in Great Britain, by Dobrivojevic and Petanovic (1982) in Macedonia, and by Csapo (1992) in Poland. The life cycle consists of a free-living phase during migration and a bud-confined phase. Mated females overwinter inside so-called "big buds" and start to lay eggs when the temperature exceeds 5~ Mites emerge when the buds are slightly open, brown and dry. Emergence takes place from early spring to early summer, and strongly depends on host plant development and climate, particularly temperature (Smith, 1962; Nielsen, 1987). Mass emergence occurs especially during and just after blossoming, during rapid shoot growth and new bud formation. In this period, the mites spread actively by crawling toward new axillary buds. They may aggregate at the base of petioles and on leaves, shortly before infesting buds. They prefer the basal and apical ones (van de Vrie, 1967). The eriophyids survive only a few days outside the buds as they are very susceptible to desiccation. Mites that emerge
Chapter 3.2.6. references, p. 588
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Currants and Berries
later in mid-summer have problems in reaching suitable new buds, as old and new buds grow apart due to elongation of the shoots. Usually only a few mites enter a bud and live on the green bud scales until the following spring. The mite population in buds increases from summer to early spring with a peak in early autumn and a second larger peak in early spring. The number of generations per year can vary from 2 to 7 (Collingwood and Brock, 1959; Savzdarg, 1957; Smith, 1961; Dobrivojevic and Petanovic, 1982).
Symptoms On black currant C. ribis causes abnormal irregular growth of buds, especially of the basal and apical ones, called "big buds". These buds become ovoid as a consequence of mite infestation. They usually dry out in the spring, either blocking the development of leaves and flowers, or producing asymmetrical and malformed leaves (Thresh, 1967). In particular, mite feeding on the meristem induces in the leaf epidermis and sometimes in the mesophyll-formation of hypertrophic cells, which are often binucleate with a hypertrophic nucleus and nucleolus (Westphal, 1977). The galls are not formed when action of the mites is interrupted during the first 4 days of infestation (Thresh, 1964a).
Biological control Predation on C. ribis has been rarely studied. Larvae of the eulophid Tetrastichus eriophyes (Taylor) were frequently observed in the field preying on eriophyoid mites inside buds (Massee, 1928; Smith, 1961). For phytoseiids such observations have not been reported in the literature, but predation seems certainly possible. For example, the phytoseiids Amblyseius aberrans (Oud.), A. finlandicus Oud. (Schausberger, 1992) and Typhlodromus pyri Scheuten (Zemek, 1993) can be reared on big bud mites. Parasitisation by fungal pathogens may well have an impact on C. ribis populations. Kanagaratnam et al. (1981) presume that Verticillium lecanii (Zimm.) Vi6gas, Macrosiphoniella sanborni (Gillette), Hirsutella thompsonii Fisher and Metarhizium anisopliae (Metsch.) Sorok. are effective pathogens of C. ribis.
Pest management Infestations of C. ribis may reduce fruit yield not only due to bud destruction, but also due to transmission of the "black currant reversion virus" which induces plant sterility. Black currant reversion and C. ribis infestation are usually found in association (Amos et al., 1927; Massee, 1952; Thresh, 1963, 1967; Proeseler, 1973; Jacob, 1976; see also Chapter 1.4.9 (Oldfield and Proeseler, 1996)) and virus-infected bushes are more susceptible to C. ribis than healthy ones (Tresh, 1967). All active instars can transmit the virus, which is acquired already after 3 h of feeding on infected bushes, with an optimum acquisition period of 50 h. Once acquired, transmission may occur after 48 h feeding on healthy bushes (Jacob, 1976). The mites may retain the virus for 25 days. Vertical transmission does not occur. Chemical treatments can be applied most effectively during spring mite dispersal, when the mites are not hidden, albeit only for a few days. Spraying is usually advised at opening of the first flowers, at the end of blossoming and during the migration period of the mites (Predki et al., 1986; Nielsen, 1987). Post-harvest sprayings have not been effective (Nielsen, 1986). Hot-water treatments of dormant black currant cuttings do not effectively control the mite, nor the reversion virus (Thresh, 1964b; Smolarz and Pala, 1982).
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de Lillo and Duso
Transfer of C. ribis from black currant to other host plants revealed mite-resistant Ribes species and varieties, used for crossing with black currant cultivars (Anderson, 1971; Proeseler, 1973; Knight et al., 1974; Easterbrook, 1980; Potapenko, 1985). In gooseberry varieties resistance is due to antixenosis, whereas in red currant it is due to antibiosis (Herr, 1988, 1991). The resistant varieties showed a low concentration of phenolic compounds in the bud tissues (see also Ostreiko and Drozdovskii, 1986; Herr, 1986), and are characterized by qualitatively different terpenoids (Brennan et al., 1992).
ERIOPHYOIDS
OF BLUEBERRY
Acalitus vaccinii
Until now 8 species of eriophyoid mites have been found on Vaccinium spp. (Amrine and Stasny, 1994). Acalitus vaccinii (Keifer), the so-called "blueberry bud mite", appears to be the major pest of wild and cultivated blueberry in North America (Keifer, 1941). It was first placed in Eriophyes (Keifer, 1939), then in Aceria (Keifer, 1946) and finally in A c a l i t u s (Baker and Neunzig, 1970). A detailed morphological description was given by Keifer (1939).
Bionomics The biology of the blueberry bud mite has been studied especially by Keifer (1941) and Baker and Neunzig (1970) in North America. Females overwinter mainly in the outer fruit bud scales, less frequently under the short basal nodes, and rarely inside the buds (Fulton, 1940). In early spring, during swelling of the blossom buds, they crawl to the bases of all bud scales and stay on the blossom clusters which develop into rosettes. Next generations can be found between the scales of rosettes or in similarly protected areas. Usually in early summer, mites leave the dried rosettes and move first to various sheltered places and in late summer to new terminal fruit buds, which are then larger than leaf buds. The mites can also be found between the corolla and calyx of flowers and sometimes on developing fruits. The population declines in summer, then gradually increases, reaching a maximum in winter when it is concentrated in the more terminal buds. Little information is available on life history parameters. Egg-to-adult development requires at least 15 days at 19~ (Baker and Neunzig, 1970). Symptoms Acalitus vaccinii causes more severe symptoms on cultivated blueberry than on wild Vaccinium species. It induces rosette-like formation of fruit buds, which is especially conspicuous in spring due to swelling of the outer scales, the epidermis of which turns reddish and is roughened or blistered. The rosettes usually hang at the base of the fruit stem; they were referred to as pseudo-galls by Keifer (1941). Infested fruit buds can develop deformed flowers or relatively normal berries (Jeppson et al., 1975). Sometimes the severely injured fruit buds may fail to bloom in late spring. Calyx and petals may partly fuse, may have a red blistered roughened surface and produce deformed berries. The fruit stems are usually watery blistered, have affected epidermes, retain the red colour of
Currants and Berries
586
growing tissues and, when badly curled, cannot produce any fruits. Delayed leaf growth can also be observed (Jeppson et al., 1975).
Biological control Several predatory mites and insects have been found in association with the blueberry bud mite (Baker and Neunzig, 1970), but none of them provided effective control. Other reports on associations with blueberry bud mites include the fungus Hirsutella thompsonii (Baker and Neunzig, 1968), but its efficacy has not yet been investigated. Pest management Keifer (1941) and Neunzig and Galletta (1977) found many cultivated and wild Vaccinium species/varieties to be susceptible to the blueberry bud mite. Others were free of blueberry bud mites which may indicate resistance. Successful chemical control may be achieved by spraying during the mites' migration period but also during the post-harvest period (Bailey and Bourne, 1946; Tomlinson, 1950). ERIOPHYOIDS
OF OTHER BERRIES
So far 31 species of eriophyoids have been reported from blackberry, raspberry and other berries. The most injurious pests are Phyllocoptes gracilis (Nalepa) and Acalitus essigi (Hassan) (Amrine and Stasny, 1994).
Phyllocoptes gracilis This species occurs widespread in Europe and North America. It lives on wild and cultivated Rubus spp. and is usually called the "raspberry leaf and bud mite". It was at first classified in the genus Cecidophyes (Nalepa, 1891), then in Eriophyes (Nalepa, 1898) and finally in Phyllocoptes (Breakey, 1945). A morphological description was provided by Nalepa (1891).
Bionomics The biology of P. gracilis has been studied mainly by Domes (1957) in Germany and by Gordon and Taylor (1976) in Scotland. Females overwinter under bud scales and in petiole scars, and less frequently in crevices of the primocanes. When the hosts sprout, the mites emerge from their overwintering sites and migrate mainly to new shoots (fructo-canes) and to new leaves where they live freely within the layer of leaf hairs. When these leaves mature, the mites move to leaves of the primo-canes. Usually, the berries become infested when mite density on leaves is very high. Starting from early autumn, at the beginning of leaf-fall, the mites move to overwintering sites. The density of the mite population increases during spring and summer, reaching a maximum in mid-summer on the fructo-canes (at the ripening of fruit) and in early autumn on the primo-canes. The life cycle is completed in 14 days at 25~ and the mite can develop many generations per year. Symptoms The type of symptoms may depend on the Rubus species under attack (raspberry, blackberry, loganberry, Himalaya berry, thimbleberry), the time of infestation and the environmental conditions (Domes, 1957; Gordon and Taylor, 1976). Leaves of raspberry infested early during development first show pale green areas that may coalesce, and later conspicuous and irregular chlorotic spots or blotches that turn into reddish necrotic areas. When infesta-
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tions are severe, growing leaves may become deformed and twisted, but mature leaves exhibit less evident symptoms. On berries, mite infestation causes more rapid development of drupelets, premature ripening and drying. Sometimes, the terminal growing points die off, followed by development of lateral buds. On infested tayberry (a blackberry x raspberry hybrid) reduction of the leaf lamina has been observed in addition to the more typical leaf symptoms (Jones et al. , 1984).
Biological control Virtually nothing is known about the efficacy of natural enemies in controlling P. gracilis. Breakey and Batchelor (1957) reported predation by phytoseiid mites, and Gordon and Taylor (1976) suspected predation by T. pyri.
Pest management When populations remain large for several years, economically important reduction of plant vigour and fruit quality may occur. Populations reach a larger size on host plants growing in sheltered areas, possibly because these favour host plant growth and thereby mite development (Gordon, 1981). So far, only few resistant varieties are available. Chemical treatments should be applied in spring when buds increase in size, and in summer just before the opening of flower buds, which helps to prevent attacks on young fruit (Gordon and Taylor, 1977; Jones et al., 1984).
Acalitus essigi This species commonly occurs on several wild and cultivated berries, especially blackberry. This so-called "blackberry mite" was first placed in Eriophyes (Hassan, 1928), then in Aceria (Keifer, 1946) and finally in A c a l i t u s (Keifer, 1965). It is widespread in Europe, North America and New Zealand (Jeppson et al., 1975). A morphological description was provided by Hassan (1928).
Bionomics The life cycle is described by Hanson (1930, 1933) and Borgman (1950). Blackberry mites overwinter in crevices around bud scales, between the petioles and stems, between bud scales and occasionally on damaged fruits. They emerge from early spring onwards and move towards the developing flowers, green berries and the bases of leaves. They live between drupelets of the berries until late summer or early winter, when they migrate back towards overwintering sites, or stay on the berries until these start to rot. Population density generally reaches its maximum in late summer or early autumn on fruits, and then decreases during winter and early spring. No quantitative information is available on number of generations per year and developmental times. Symptoms Apart from blackberry, A. essigi has been found also on Himalaya berry, boysenberry, raspberry, loganberry and other Rubus spp. (Hanson, 1930; Borgman, 1950; Keifer et al., 1982). Its feeding activity causes the "redberry disease", consisting of an incomplete, delayed and uneven ripening of the berries, especially in late maturing varieties. The infested berries show swollen, brilliant red or pink and greenish drupelets among the normal maroon or black drupelets. They gradually fade and dry out in autumn and winter. Highly infested berries may be completely red.
Currants and Berries
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Biological control Little is k n o w n about the efficacy of natural enemies in controlling the blackberry mite. Hanson (1933) reported predation of phytoseiid mites on A. essigi. Pest m a n a g e m e n t Mite infestations may cause high yield loss because fruits become unmarketable. Late maturing varieties may incur more damage, as their fruits are more exposed to mite attack. To effectively control the mite, 2 to 3 sprayings before flowering are advised (Krczal, 1966; Alford, 1979; Bolay et al., 1989).
FUTURE
RESEARCH
NEEDS
Current knowledge of the life cycle of eriophyoid mites on currants and berries is fragmentary. This clearly needs more investigation, in order to assess the number of generations per year and to determine dispersal within and between plants. Especially, the life cycle of A. essigi should be unravelled as it is the most poorly understood. Also, the few eriophyoid species known to occur on strawberries deserve priority for further research, as they are virtually unexplored with respect to life cycle and pest status. The selection and implementation of resistant cultivars for pest management seems a promising research area. Yet, there is a need for basic research to analyse the underlying mechanisms by which host plants become resistant to eriophyoid mites. This may broaden the scope for resistance breeding. A potentially important area of future research is to investigate how virus transmission depends on population density and, in particular, whether small numbers of eriophyoid mites suffice to transmit viruses. For example, it is unknown to what extent C. ribis can survive in buds of resistant Ribes varieties and yet transmit the virus causing reversion disease. The natural enemies of eriophyoids on currants and berries have not yet been unambiguously identified, let alone their impact on the dynamics of eriophyoid mites. Research focused on the development of biological control is a major area for future research.
ACKNOWLEDGMENTS The authors are grateful to Dr. M.A. Easterbrook, HRI, East Malling, England, for critical reading of the manuscript, and to MURST for partial financial support.
REFERENCES Alford, D.V., 1979. Chemical control of blackberry mite, Acalitus essigi (Hassan). Plant Pathol., 28: 91-94. Amos, J., Hatton, R.G., Knight, R.C. and Massee, A.M., 1927. Experiments in the transmission of reversion in black currants. Ann. Rep. E. Malling Res. Sta. Kent, 13: 126-150. Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmata) of the World. Indira Publ. House, Bloomfield, Michigan, USA, 798 pp. Amrine, J.W., Jr. Duncan, G.H., Jones, A.T., Gordon, S.C. and Roberts, I.A., 1994. Cecidophyopsis mites (Acari: Eriophyidae) on Ribes spp. (Grossulariaceae). Intern. J. Acarol., 20: 139-168. Anderson, M.M., 1971. Resistance to gall mite (Phytoptus ribis Nal.) in the Eucoreosma section of Ribes. Euphytica, 20: 422-426.
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Bailey, J.S. and Bourne, A.I., 1946. The control of the Blueberry Bud Mite. J. Econ. Entomol., 39: 89. Baker, J.R. and Neunzig, H.H., 1968. Hirsutella thompsonii as a fungus parasite of the blueberry bud mite. J. Econ. Entomol., 61: 1117-1118. Baker, J.R. and Neunzig, H.H., 1970. Biology of the Blueberry Bud Mite. J. Econ. Entomol., 63: 74-79. Bolay, A., St/iubli, A., Baillod, M., Ducrot, V., Guignard, E., Antonin, Ph., Neury, G. and Terretaz, R., 1989. Guide des traitements des groseilliers et des cassis. Rev. Suisse Vitic., Arboric. Hortic., 21: 81-87. Borgman, H.H., 1950. De "rode vrucht ziekte" bij bramen, veroorzaakt door de galmijt Eriophyes essigi Hassan. Tijdschr. P1. Ziekt., 56: 149-160. Breakey, E.P., 1945. Phyllocoptes gracilis, a pest of red raspberry in the Puyallup Valley. J. Econ. Entomol., 38: 121-122. Breakey, E.P. and Batchelor, G.S., 1957. Biology and control of the Dryberry Mite, Phyllocoptes gracilis (Nal.). Bull. Wash. agric, exp. Sta., 574:17 pp. Brennan, R.M., Robertson, G.W., McNicol, J.W., Fyffe, L. and Hall, J.E., 1992. The use of metabolic profiling in the identification of gall mite (Cecidophyopsis ribis Westw.) - resistant Black Currant (Ribes nigrum L.) genotypes. Ann. Appl. Biol., 121: 503-509. Collingwood, C.A. and Brock, A.M., 1959. Ecology of the black currant gall mite (Phytoptus ribis Nal.). J. Hort. Sci., 34: 176-182. Csapo, Z., 1992. Eriophyid mites (Acarina-Eriophyoidea) on currants: morphology, taxonomy and ecology. Ph.D. Thesis, Warsaw Agric. Univ., Warsaw, Poland, 112 pp. Dobrivojevic, K. and Petanovic R., 1982. Grinja ribizlinog pupoljka (Cecidophyopsis ribis Westwood, Eriophyidae, Acarina) i njena uloga u propadanju zasada crne ribizle. Zastita Bilja, 33: 507-518. Domes, R., 1957. Zur Biologie der Gallmilbe Eriophyes gracilis Nalepa. Z. Angew. Entomol., 41: 411-424. Easterbrook, M.A., 1980. The host range of a "non-gall-forming" eriophyid mite living in buds on Ribes. J. Hort. Sci., 55: 1-6. Fenton, B., Malloch, G., Jones, A.T., Birch, A.N.E., Gordon, S.C., A'Hara, S., McGavin, W.J. and Amrine, J.W., Jr.,, 1995. Species identification of Cecidophyopsis mites (Acari: Eriophyidae) from different Ribes species and countries using molecular genetics. Molecular Ecology, 4: 383-387. Fulton, B.B., 1940. The Blueberry Bud Mite, a new pest. J. Econ. Entomol., 33: 699. Gordon, S.C., 1981. Raspberry leaf and bud mite. Leaflet, Min. Agric., Fish Food, n. 790:5 PP. Gordon, S.C. and Taylor, C.E., 1976. Some aspects of the biology of the raspberry leaf and bud mite (Phyllocoptes (Eriophyes) gracilis Nal.) Eriophyidae in Scotland. J. Hort. Sci., 51: 501-508. Gordon, S.C. and Taylor, C.E., 1977. Chemical control of the raspberry leaf and bud mite, Phyllocoptes gracilis (Nal.) (Eriophyidae). J. Hort. Sci., 52: 517-523. Hanson, A.J., 1930. The Redberry disease of Blackberries. Proc. Washington St. Hort. Ass., 26: 199-201. Hanson, A.J., 1933. The Blackberry Mite and its control (Eriophyes essigi Hassan). Bull. Wash. Agric. Expt. Sta., 279: 1-20. Hassan, A.S., 1928. The biology of the Eriophyidae with special reference to Eriophyes tristriatus (Nalepa). Cal. Univ. Publ. Entomol., 4: 341-394. Herr, R., 1986. Unterschungen ~iber die Resistenzmechanismen der Gattung Ribes gegen die Johannisbeergallmilbe Cecidophyopsis ribis. Mitt. Biol. Bund. Land-Fort., Berlin-Dahlem, 232: 359. Herr, R., 1988. Unterschungen zum Resistenzmechanismus der Gattung Ribes gegen die Johannisbeergallmilbe Cecidophyopsis ribis. Mitt. Deut. Gesell. All. Angew. Entomol., 6: 17-21. Herr, R., 1991. Untersuchungen zur Resistenz der Gattung Ribes gegen die Johannisbeergallmilbe, Cecidophyopsis ribis (Westw.) (Acari, Eriophyidae). Infektions-versuche und Biotests. J. Appl. Entomol., 112: 181-1293. Jacob, H., 1976. Untersuchungen zur Obertragung des vir6sen Atavismus der Schwarzen Johannisbeere (Ribes nigrum L.) durch die Gallmilbe Cecidophyopsis ribis Westw. Zeit. Pf. Pflanzen., 83: 448-458. Jeppson, L.R., Keifer, H.H. and Baker, G.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Jones, A.T., Gordon, S.C. and Jennings, D.L., 1984. A leaf-blotch disorder of tayberry associated with the leaf and bud mite (Phyllocoptes gracilis) and some effects of three aphidborne viruses. J. Hort. Sci., 59: 523-528.
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Currants and Berries Kanagaratnam, P., Hall, R.A. and Burges, H.D., 1981. Effect of fungi on the Black Currant gall mite, Cecidophyopsis ribis. Plant Pathol., 30: 117-118. Keifer, H.H., 1939. Eriophyid Studies. V. Bull. Dept. Agric. Calif., 28: 328-345. Keifer, H.H., 1941. Eriophyid Studies. XI. Bull. Dept. Agric. Calif., 30: 196-216. Keifer, H.H., 1946. A review of North American economic eriophyid mites. J. Econ. Entomol., 39: 563-570. Keifer, H.H., 1965. Eriophyid Studies. Calif. Dept. Agric., B-16: 1-20. Keifer, H.H., Baker, E.W., Kono, T., Delfinado, M. and Styer, W., 1982. An illustrated guide to plant abnormalities caused by Eriophyid Mites in North America. USDA, Agr. handbook 573, 178 pp. Knight, R.L., Keep, E., Briggs, J.B. and Parker, J.H., 1974. Transference of resistance to black currant gall mite, Cecidophyopsis ribis, from gooseberry to black currant. Ann. Appl. Biol., 76: 123-130. Krczal, H., 1966. Untersuchungen zur Bek/impfung der Brombeergallmilbe Eriophyes essigi Hassan. Bad Obst-u. Gartenbr., 12: 53-54. Massee, A.M., 1928. The life-history of the black currant gall mite, Eriophyes ribis (Westw.) Nal. Bull. Entomol. Res., 18:297-309 + 2 pls. Massee, A.M., 1952. Transmission of reversion of black currants. Ann. Rep. E. Malling Res. Sta. Kent for 1951: 162-165. Massee, A.M., 1961. The gall mites (Arachnida: Acarina: Eriophyidae) of Kent. Trans. Kent Field Club, 1: 109-119. Nalepa, A., 1891. Neue Gallmilben. Nova Acta Leop. Akad., 55: 361-395. Nalepa, A., 1893. Neue Gallmilben. 7 Fort. Anz. Akad. Wiss. Wien, 30: 105. Nalepa, A., 1898. Acarina, Eriophyidae (Phytoptidae). Das Tierreich, 4. Liefrung, 74 pp. Neunzig, H.H. and Galletta, G.J., 1977. Abundance of the Blueberry Bud Mite (Acarina, Eriophyidae) on various species of Blueberry. J. Georgia Entomol. Soc., 12: 183-184. Nielsen, S.L., 1986. Postharvest sprayings with 2 systemic pesticides against the black currant gall mite (Cecidophyopsis ribis Westw.) on black currant (Ribes nigrum). Danish J. Plant Soil Sci., 90: 385-388. Nielsen, S.L., 1987. Pesticides tested for the control of black currant gall mite (Cecidophyopsis ribis Westw.). J. Hort. Sci., 62" 27-30. Oldfield, G.N. and Proeseler, G., 1996. Eriophyoid mites as vectors of plant pathogens. In: E.E. Lindquist, M.W. Sabelis and J. Bruin (Editors), Eriophyoid mites- Their biology, natural enemies and control. Elsevier Science Publ., Amsterdam, The Netherlands, pp. 259-275. Ostreiko, S.A. and Drozdovskii, E.M., 1986. The role of phenols in the resistance of Currant to certain pathogens. In: Intensif. Pr-va yagod, Moscow: 74-84. Potapenko, A.A., 1985. Breeding black currant for a combination of economically useful characters. In: Selektsiya i agrotekhnika plodovo-yagodnykh i dekorativnykh kul'tur, Novosibirsk: 15-22. Predki, S., Suski, Z.W. and Smolarz, S., 1986. Chemical control of black currant gall mite Cecidophyopsis ribis (Westw.). Pr. Inst. Sad. Ser. A, 26: 89-95. Proeseler, G., 1973. Die Gallmilbe Cecidophyopsis ribis (Westw.) als Sch/idling der Johannisbeeren. Arch. Phytop. Pflanz., 9:383-394 + 3 pls. Savzdarg, E.E., 1957. Ways of freeing berry fruits from mites in relation to peculiarities of their biology and ecology. Izv. Timiryazer. seljsk. Akad., 1: 5-19. Schausberger, V.P., 1992. Vergleichende Untersuchungen ~iber den Einflul~ unterschiedlicher Nahrung auf die Pr/iimaginalentwicklung und die Reproduction yon Amblyseius aberrans Oud. und Amblyseius finlandicus Oud. (Acarina, Phytoseiidae). J. Appl. Entomol., 113: 476-486. Smith, B.D., 1959. The behaviour of the black currant gall mite (Phytoptus ribis Nal.) during the free living phase of its life cycle. Ann. Rep. Agric. hort. Res. Sta., Long Ashton, Bristol, for 1959: 130-136. Smith, B.D., 1961. Population studies of the black currant gall mite (Phytoptus ribis Nal.). Ann. Rep. Agric. hort. Res. Sta., Long Ashton, Bristol, for 1960: 120-124. Smith, B.D., 1962. The behaviour and control of the black currant gall mite Phytoptus ribis (Nal.). Ann. Appl. Biol., 50: 327-334. Smolarz, S. and Pala, E., 1982. Thermic method of gall mite control in buds of black currants. Pra. Inst. Sad. Ser. A, 23: 131-135. Thresh, J.M., 1963. A vein pattern of Black Currant leaves associated with reversion disease. Ann. Rep. E. Malling Res. Sta., Kent, for 1962: 97-98. Thresh, J.M., 1964a. Association between black currant reversion virus and its gall mite vector. Nature 202: 1085-1087. Thresh, J.M., 1964b. Warm water treatments to eliminate the gall mite Phytoptus ribis Nal. from Black Currant cuttings. Ann. Rep. E. Malling Res. Sta., Kent, for 1963: 131-132.
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Thresh, J.M., 1967. Increased susceptibility of Black-Currant bushes to the Gall-mite vector (Phytoptus ribis Nal.) following infection with reversion virus. Ann. Appl. Biol., 60: 455-467. Tomlinson, W.E., 1950. Summer oil sprays to control Blueberry Bud Mite. J. Econ. Entomol., 43: 727. van de Vrie, M., 1967. De levenswijze en de bestrijding van de rondknopmijt van zwarte bes Cecidophyopsis ribis. Neth. J. P1. Path., 73: 170-180. Westphal, E., 1977. Morphogen~se, ultrastructure et ~tiologie de quelques galles d'Erio phyes (Acariens). Marcellia, 39: 193-375. Zemek, R., 1993. Characteristics of development and reproduction in Typhlodromus pyri on Tetranychus urticae and Cecidophyopsis ribis. I. Overwintered females. Exp. Appl. Acarol., 17: 405-421.
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3.2.6 Currants and Berries E. DE LILLO and C. DUSO
Eriophyoids are of economic importance in cultures of various small fruits (e.g., black and red currants, blueberry, blackberry). In this chapter their biology, injuriousness, natural enemies and pest management are discussed.
ERIOPHYOIDS
OF CURRANTS
Until now 18 species of eriophyoids have been found on Ribes spp., the majority on black currant, R. nigrum L. (Amrine and Stasny, 1994; Amrine et al., 1994). Recently, Amrine et al. (1994) reviewed closely-related species in the genus Cecidophyopsis occurring on Ribes spp. showing significant morphological differences. Moreover, they reviewed their geographical distribution, biology and host relationships, revealing a high specificity for individual species of Ribes confirmed by molecular evidence of the mite ribosomal DNA (Fenton et al., 1995). Among these species, C. ribis (Westwood) appears to be the most noxious, as it causes direct damage to the buds and indirect damage to the plant.
Cecidophyopsi$ ribis This species occurs mainly in Europe and is commonly called "black currant bud mite" or "big bud mite". It was previously known under the generic names P h y t o p t u s (Nalepa, 1893), Eriophyes (Nalepa, 1898), Cecidophyes (Keifer, 1946) and finally Cecidophyopsis (Massee, 1961). Bionomics The biology of the big bud mite has been studied by Massee (1928), Collingwood and Brock (1959), Smith (1959, 1961) and Thresh (1967) in Great Britain, by Dobrivojevic and Petanovic (1982) in Macedonia, and by Csapo (1992) in Poland. The life cycle consists of a free-living phase during migration and a bud-confined phase. Mated females overwinter inside so-called "big buds" and start to lay eggs when the temperature exceeds 5~ Mites emerge when the buds are slightly open, brown and dry. Emergence takes place from early spring to early summer, and strongly depends on host plant development and climate, particularly temperature (Smith, 1962; Nielsen, 1987). Mass emergence occurs especially during and just after blossoming, during rapid shoot growth and new bud formation. In this period, the mites spread actively by crawling toward new axillary buds. They may aggregate at the base of petioles and on leaves, shortly before infesting buds. They prefer the basal and apical ones (van de Vrie, 1967). The eriophyids survive only a few days outside the buds as they are very susceptible to desiccation. Mites that emerge
Chapter 3.2.6. references, p. 588
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Currants and Berries
later in mid-summer have problems in reaching suitable new buds, as old and new buds grow apart due to elongation of the shoots. Usually only a few mites enter a bud and live on the green bud scales until the following spring. The mite population in buds increases from summer to early spring with a peak in early autumn and a second larger peak in early spring. The number of generations per year can vary from 2 to 7 (Collingwood and Brock, 1959; Savzdarg, 1957; Smith, 1961; Dobrivojevic and Petanovic, 1982).
Symptoms On black currant C. ribis causes abnormal irregular growth of buds, especially of the basal and apical ones, called "big buds". These buds become ovoid as a consequence of mite infestation. They usually dry out in the spring, either blocking the development of leaves and flowers, or producing asymmetrical and malformed leaves (Thresh, 1967). In particular, mite feeding on the meristem induces in the leaf epidermis and sometimes in the mesophyll-formation of hypertrophic cells, which are often binucleate with a hypertrophic nucleus and nucleolus (Westphal, 1977). The galls are not formed when action of the mites is interrupted during the first 4 days of infestation (Thresh, 1964a).
Biological control Predation on C. ribis has been rarely studied. Larvae of the eulophid Tetrastichus eriophyes (Taylor) were frequently observed in the field preying on eriophyoid mites inside buds (Massee, 1928; Smith, 1961). For phytoseiids such observations have not been reported in the literature, but predation seems certainly possible. For example, the phytoseiids Amblyseius aberrans (Oud.), A. finlandicus Oud. (Schausberger, 1992) and Typhlodromus pyri Scheuten (Zemek, 1993) can be reared on big bud mites. Parasitisation by fungal pathogens may well have an impact on C. ribis populations. Kanagaratnam et al. (1981) presume that Verticillium lecanii (Zimm.) Vi6gas, Macrosiphoniella sanborni (Gillette), Hirsutella thompsonii Fisher and Metarhizium anisopliae (Metsch.) Sorok. are effective pathogens of C. ribis.
Pest management Infestations of C. ribis may reduce fruit yield not only due to bud destruction, but also due to transmission of the "black currant reversion virus" which induces plant sterility. Black currant reversion and C. ribis infestation are usually found in association (Amos et al., 1927; Massee, 1952; Thresh, 1963, 1967; Proeseler, 1973; Jacob, 1976; see also Chapter 1.4.9 (Oldfield and Proeseler, 1996)) and virus-infected bushes are more susceptible to C. ribis than healthy ones (Tresh, 1967). All active instars can transmit the virus, which is acquired already after 3 h of feeding on infected bushes, with an optimum acquisition period of 50 h. Once acquired, transmission may occur after 48 h feeding on healthy bushes (Jacob, 1976). The mites may retain the virus for 25 days. Vertical transmission does not occur. Chemical treatments can be applied most effectively during spring mite dispersal, when the mites are not hidden, albeit only for a few days. Spraying is usually advised at opening of the first flowers, at the end of blossoming and during the migration period of the mites (Predki et al., 1986; Nielsen, 1987). Post-harvest sprayings have not been effective (Nielsen, 1986). Hot-water treatments of dormant black currant cuttings do not effectively control the mite, nor the reversion virus (Thresh, 1964b; Smolarz and Pala, 1982).
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Transfer of C. ribis from black currant to other host plants revealed mite-resistant Ribes species and varieties, used for crossing with black currant cultivars (Anderson, 1971; Proeseler, 1973; Knight et al., 1974; Easterbrook, 1980; Potapenko, 1985). In gooseberry varieties resistance is due to antixenosis, whereas in red currant it is due to antibiosis (Herr, 1988, 1991). The resistant varieties showed a low concentration of phenolic compounds in the bud tissues (see also Ostreiko and Drozdovskii, 1986; Herr, 1986), and are characterized by qualitatively different terpenoids (Brennan et al., 1992).
ERIOPHYOIDS
OF BLUEBERRY
Acalitus vaccinii
Until now 8 species of eriophyoid mites have been found on Vaccinium spp. (Amrine and Stasny, 1994). Acalitus vaccinii (Keifer), the so-called "blueberry bud mite", appears to be the major pest of wild and cultivated blueberry in North America (Keifer, 1941). It was first placed in Eriophyes (Keifer, 1939), then in Aceria (Keifer, 1946) and finally in A c a l i t u s (Baker and Neunzig, 1970). A detailed morphological description was given by Keifer (1939).
Bionomics The biology of the blueberry bud mite has been studied especially by Keifer (1941) and Baker and Neunzig (1970) in North America. Females overwinter mainly in the outer fruit bud scales, less frequently under the short basal nodes, and rarely inside the buds (Fulton, 1940). In early spring, during swelling of the blossom buds, they crawl to the bases of all bud scales and stay on the blossom clusters which develop into rosettes. Next generations can be found between the scales of rosettes or in similarly protected areas. Usually in early summer, mites leave the dried rosettes and move first to various sheltered places and in late summer to new terminal fruit buds, which are then larger than leaf buds. The mites can also be found between the corolla and calyx of flowers and sometimes on developing fruits. The population declines in summer, then gradually increases, reaching a maximum in winter when it is concentrated in the more terminal buds. Little information is available on life history parameters. Egg-to-adult development requires at least 15 days at 19~ (Baker and Neunzig, 1970). Symptoms Acalitus vaccinii causes more severe symptoms on cultivated blueberry than on wild Vaccinium species. It induces rosette-like formation of fruit buds, which is especially conspicuous in spring due to swelling of the outer scales, the epidermis of which turns reddish and is roughened or blistered. The rosettes usually hang at the base of the fruit stem; they were referred to as pseudo-galls by Keifer (1941). Infested fruit buds can develop deformed flowers or relatively normal berries (Jeppson et al., 1975). Sometimes the severely injured fruit buds may fail to bloom in late spring. Calyx and petals may partly fuse, may have a red blistered roughened surface and produce deformed berries. The fruit stems are usually watery blistered, have affected epidermes, retain the red colour of
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growing tissues and, when badly curled, cannot produce any fruits. Delayed leaf growth can also be observed (Jeppson et al., 1975).
Biological control Several predatory mites and insects have been found in association with the blueberry bud mite (Baker and Neunzig, 1970), but none of them provided effective control. Other reports on associations with blueberry bud mites include the fungus Hirsutella thompsonii (Baker and Neunzig, 1968), but its efficacy has not yet been investigated. Pest management Keifer (1941) and Neunzig and Galletta (1977) found many cultivated and wild Vaccinium species/varieties to be susceptible to the blueberry bud mite. Others were free of blueberry bud mites which may indicate resistance. Successful chemical control may be achieved by spraying during the mites' migration period but also during the post-harvest period (Bailey and Bourne, 1946; Tomlinson, 1950). ERIOPHYOIDS
OF OTHER BERRIES
So far 31 species of eriophyoids have been reported from blackberry, raspberry and other berries. The most injurious pests are Phyllocoptes gracilis (Nalepa) and Acalitus essigi (Hassan) (Amrine and Stasny, 1994).
Phyllocoptes gracilis This species occurs widespread in Europe and North America. It lives on wild and cultivated Rubus spp. and is usually called the "raspberry leaf and bud mite". It was at first classified in the genus Cecidophyes (Nalepa, 1891), then in Eriophyes (Nalepa, 1898) and finally in Phyllocoptes (Breakey, 1945). A morphological description was provided by Nalepa (1891).
Bionomics The biology of P. gracilis has been studied mainly by Domes (1957) in Germany and by Gordon and Taylor (1976) in Scotland. Females overwinter under bud scales and in petiole scars, and less frequently in crevices of the primocanes. When the hosts sprout, the mites emerge from their overwintering sites and migrate mainly to new shoots (fructo-canes) and to new leaves where they live freely within the layer of leaf hairs. When these leaves mature, the mites move to leaves of the primo-canes. Usually, the berries become infested when mite density on leaves is very high. Starting from early autumn, at the beginning of leaf-fall, the mites move to overwintering sites. The density of the mite population increases during spring and summer, reaching a maximum in mid-summer on the fructo-canes (at the ripening of fruit) and in early autumn on the primo-canes. The life cycle is completed in 14 days at 25~ and the mite can develop many generations per year. Symptoms The type of symptoms may depend on the Rubus species under attack (raspberry, blackberry, loganberry, Himalaya berry, thimbleberry), the time of infestation and the environmental conditions (Domes, 1957; Gordon and Taylor, 1976). Leaves of raspberry infested early during development first show pale green areas that may coalesce, and later conspicuous and irregular chlorotic spots or blotches that turn into reddish necrotic areas. When infesta-
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tions are severe, growing leaves may become deformed and twisted, but mature leaves exhibit less evident symptoms. On berries, mite infestation causes more rapid development of drupelets, premature ripening and drying. Sometimes, the terminal growing points die off, followed by development of lateral buds. On infested tayberry (a blackberry x raspberry hybrid) reduction of the leaf lamina has been observed in addition to the more typical leaf symptoms (Jones et al. , 1984).
Biological control Virtually nothing is known about the efficacy of natural enemies in controlling P. gracilis. Breakey and Batchelor (1957) reported predation by phytoseiid mites, and Gordon and Taylor (1976) suspected predation by T. pyri.
Pest management When populations remain large for several years, economically important reduction of plant vigour and fruit quality may occur. Populations reach a larger size on host plants growing in sheltered areas, possibly because these favour host plant growth and thereby mite development (Gordon, 1981). So far, only few resistant varieties are available. Chemical treatments should be applied in spring when buds increase in size, and in summer just before the opening of flower buds, which helps to prevent attacks on young fruit (Gordon and Taylor, 1977; Jones et al., 1984).
Acalitus essigi This species commonly occurs on several wild and cultivated berries, especially blackberry. This so-called "blackberry mite" was first placed in Eriophyes (Hassan, 1928), then in Aceria (Keifer, 1946) and finally in A c a l i t u s (Keifer, 1965). It is widespread in Europe, North America and New Zealand (Jeppson et al., 1975). A morphological description was provided by Hassan (1928).
Bionomics The life cycle is described by Hanson (1930, 1933) and Borgman (1950). Blackberry mites overwinter in crevices around bud scales, between the petioles and stems, between bud scales and occasionally on damaged fruits. They emerge from early spring onwards and move towards the developing flowers, green berries and the bases of leaves. They live between drupelets of the berries until late summer or early winter, when they migrate back towards overwintering sites, or stay on the berries until these start to rot. Population density generally reaches its maximum in late summer or early autumn on fruits, and then decreases during winter and early spring. No quantitative information is available on number of generations per year and developmental times. Symptoms Apart from blackberry, A. essigi has been found also on Himalaya berry, boysenberry, raspberry, loganberry and other Rubus spp. (Hanson, 1930; Borgman, 1950; Keifer et al., 1982). Its feeding activity causes the "redberry disease", consisting of an incomplete, delayed and uneven ripening of the berries, especially in late maturing varieties. The infested berries show swollen, brilliant red or pink and greenish drupelets among the normal maroon or black drupelets. They gradually fade and dry out in autumn and winter. Highly infested berries may be completely red.
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Biological control Little is k n o w n about the efficacy of natural enemies in controlling the blackberry mite. Hanson (1933) reported predation of phytoseiid mites on A. essigi. Pest m a n a g e m e n t Mite infestations may cause high yield loss because fruits become unmarketable. Late maturing varieties may incur more damage, as their fruits are more exposed to mite attack. To effectively control the mite, 2 to 3 sprayings before flowering are advised (Krczal, 1966; Alford, 1979; Bolay et al., 1989).
FUTURE
RESEARCH
NEEDS
Current knowledge of the life cycle of eriophyoid mites on currants and berries is fragmentary. This clearly needs more investigation, in order to assess the number of generations per year and to determine dispersal within and between plants. Especially, the life cycle of A. essigi should be unravelled as it is the most poorly understood. Also, the few eriophyoid species known to occur on strawberries deserve priority for further research, as they are virtually unexplored with respect to life cycle and pest status. The selection and implementation of resistant cultivars for pest management seems a promising research area. Yet, there is a need for basic research to analyse the underlying mechanisms by which host plants become resistant to eriophyoid mites. This may broaden the scope for resistance breeding. A potentially important area of future research is to investigate how virus transmission depends on population density and, in particular, whether small numbers of eriophyoid mites suffice to transmit viruses. For example, it is unknown to what extent C. ribis can survive in buds of resistant Ribes varieties and yet transmit the virus causing reversion disease. The natural enemies of eriophyoids on currants and berries have not yet been unambiguously identified, let alone their impact on the dynamics of eriophyoid mites. Research focused on the development of biological control is a major area for future research.
ACKNOWLEDGMENTS The authors are grateful to Dr. M.A. Easterbrook, HRI, East Malling, England, for critical reading of the manuscript, and to MURST for partial financial support.
REFERENCES Alford, D.V., 1979. Chemical control of blackberry mite, Acalitus essigi (Hassan). Plant Pathol., 28: 91-94. Amos, J., Hatton, R.G., Knight, R.C. and Massee, A.M., 1927. Experiments in the transmission of reversion in black currants. Ann. Rep. E. Malling Res. Sta. Kent, 13: 126-150. Amrine, J.W., Jr. and Stasny, T.A., 1994. Catalog of the Eriophyoidea (Acarina: Prostigmata) of the World. Indira Publ. House, Bloomfield, Michigan, USA, 798 pp. Amrine, J.W., Jr. Duncan, G.H., Jones, A.T., Gordon, S.C. and Roberts, I.A., 1994. Cecidophyopsis mites (Acari: Eriophyidae) on Ribes spp. (Grossulariaceae). Intern. J. Acarol., 20: 139-168. Anderson, M.M., 1971. Resistance to gall mite (Phytoptus ribis Nal.) in the Eucoreosma section of Ribes. Euphytica, 20: 422-426.
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Bailey, J.S. and Bourne, A.I., 1946. The control of the Blueberry Bud Mite. J. Econ. Entomol., 39: 89. Baker, J.R. and Neunzig, H.H., 1968. Hirsutella thompsonii as a fungus parasite of the blueberry bud mite. J. Econ. Entomol., 61: 1117-1118. Baker, J.R. and Neunzig, H.H., 1970. Biology of the Blueberry Bud Mite. J. Econ. Entomol., 63: 74-79. Bolay, A., St/iubli, A., Baillod, M., Ducrot, V., Guignard, E., Antonin, Ph., Neury, G. and Terretaz, R., 1989. Guide des traitements des groseilliers et des cassis. Rev. Suisse Vitic., Arboric. Hortic., 21: 81-87. Borgman, H.H., 1950. De "rode vrucht ziekte" bij bramen, veroorzaakt door de galmijt Eriophyes essigi Hassan. Tijdschr. P1. Ziekt., 56: 149-160. Breakey, E.P., 1945. Phyllocoptes gracilis, a pest of red raspberry in the Puyallup Valley. J. Econ. Entomol., 38: 121-122. Breakey, E.P. and Batchelor, G.S., 1957. Biology and control of the Dryberry Mite, Phyllocoptes gracilis (Nal.). Bull. Wash. agric, exp. Sta., 574:17 pp. Brennan, R.M., Robertson, G.W., McNicol, J.W., Fyffe, L. and Hall, J.E., 1992. The use of metabolic profiling in the identification of gall mite (Cecidophyopsis ribis Westw.) - resistant Black Currant (Ribes nigrum L.) genotypes. Ann. Appl. Biol., 121: 503-509. Collingwood, C.A. and Brock, A.M., 1959. Ecology of the black currant gall mite (Phytoptus ribis Nal.). J. Hort. Sci., 34: 176-182. Csapo, Z., 1992. Eriophyid mites (Acarina-Eriophyoidea) on currants: morphology, taxonomy and ecology. Ph.D. Thesis, Warsaw Agric. Univ., Warsaw, Poland, 112 pp. Dobrivojevic, K. and Petanovic R., 1982. Grinja ribizlinog pupoljka (Cecidophyopsis ribis Westwood, Eriophyidae, Acarina) i njena uloga u propadanju zasada crne ribizle. Zastita Bilja, 33: 507-518. Domes, R., 1957. Zur Biologie der Gallmilbe Eriophyes gracilis Nalepa. Z. Angew. Entomol., 41: 411-424. Easterbrook, M.A., 1980. The host range of a "non-gall-forming" eriophyid mite living in buds on Ribes. J. Hort. Sci., 55: 1-6. Fenton, B., Malloch, G., Jones, A.T., Birch, A.N.E., Gordon, S.C., A'Hara, S., McGavin, W.J. and Amrine, J.W., Jr.,, 1995. Species identification of Cecidophyopsis mites (Acari: Eriophyidae) from different Ribes species and countries using molecular genetics. Molecular Ecology, 4: 383-387. Fulton, B.B., 1940. The Blueberry Bud Mite, a new pest. J. Econ. Entomol., 33: 699. Gordon, S.C., 1981. Raspberry leaf and bud mite. Leaflet, Min. Agric., Fish Food, n. 790:5 PP. Gordon, S.C. and Taylor, C.E., 1976. Some aspects of the biology of the raspberry leaf and bud mite (Phyllocoptes (Eriophyes) gracilis Nal.) Eriophyidae in Scotland. J. Hort. Sci., 51: 501-508. Gordon, S.C. and Taylor, C.E., 1977. Chemical control of the raspberry leaf and bud mite, Phyllocoptes gracilis (Nal.) (Eriophyidae). J. Hort. Sci., 52: 517-523. Hanson, A.J., 1930. The Redberry disease of Blackberries. Proc. Washington St. Hort. Ass., 26: 199-201. Hanson, A.J., 1933. The Blackberry Mite and its control (Eriophyes essigi Hassan). Bull. Wash. Agric. Expt. Sta., 279: 1-20. Hassan, A.S., 1928. The biology of the Eriophyidae with special reference to Eriophyes tristriatus (Nalepa). Cal. Univ. Publ. Entomol., 4: 341-394. Herr, R., 1986. Unterschungen ~iber die Resistenzmechanismen der Gattung Ribes gegen die Johannisbeergallmilbe Cecidophyopsis ribis. Mitt. Biol. Bund. Land-Fort., Berlin-Dahlem, 232: 359. Herr, R., 1988. Unterschungen zum Resistenzmechanismus der Gattung Ribes gegen die Johannisbeergallmilbe Cecidophyopsis ribis. Mitt. Deut. Gesell. All. Angew. Entomol., 6: 17-21. Herr, R., 1991. Untersuchungen zur Resistenz der Gattung Ribes gegen die Johannisbeergallmilbe, Cecidophyopsis ribis (Westw.) (Acari, Eriophyidae). Infektions-versuche und Biotests. J. Appl. Entomol., 112: 181-1293. Jacob, H., 1976. Untersuchungen zur Obertragung des vir6sen Atavismus der Schwarzen Johannisbeere (Ribes nigrum L.) durch die Gallmilbe Cecidophyopsis ribis Westw. Zeit. Pf. Pflanzen., 83: 448-458. Jeppson, L.R., Keifer, H.H. and Baker, G.W., 1975. Mites injurious to economic plants. University of California Press, Berkeley, California, USA, 614 pp. Jones, A.T., Gordon, S.C. and Jennings, D.L., 1984. A leaf-blotch disorder of tayberry associated with the leaf and bud mite (Phyllocoptes gracilis) and some effects of three aphidborne viruses. J. Hort. Sci., 59: 523-528.
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Thresh, J.M., 1967. Increased susceptibility of Black-Currant bushes to the Gall-mite vector (Phytoptus ribis Nal.) following infection with reversion virus. Ann. Appl. Biol., 60: 455-467. Tomlinson, W.E., 1950. Summer oil sprays to control Blueberry Bud Mite. J. Econ. Entomol., 43: 727. van de Vrie, M., 1967. De levenswijze en de bestrijding van de rondknopmijt van zwarte bes Cecidophyopsis ribis. Neth. J. P1. Path., 73: 170-180. Westphal, E., 1977. Morphogen~se, ultrastructure et ~tiologie de quelques galles d'Erio phyes (Acariens). Marcellia, 39: 193-375. Zemek, R., 1993. Characteristics of development and reproduction in Typhlodromus pyri on Tetranychus urticae and Cecidophyopsis ribis. I. Overwintered females. Exp. Appl. Acarol., 17: 405-421.