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Coccid Pests of Important Crops
Soft Scale Insects - Their Biology, Natural Enemies and Control (7B) Y. Ben-Dov and C.J. Hodgson (Editors) 1997 Elsevier Science B.V.
Chapter 3.3 Crops 3.3.1
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Citrus
RAYMOND J. GILL
INTRODUCTION The citrus fruit, because of its attractiveness, good taste and nutritive value, has gained popularity with peoples all over the globe. Trees of certain Citrus varieties are attractive in their own fight and have been used in ornamental landscaping. The leaves of particular varieties are used as a spice, particularly with chicken dishes and, in some cultures, the rind is used medicinally. The major commercial citrus species that are currently being grown (Snowdon, 1990; Whiteside, 1988) include sweet orange, Citrus sinensis, mandarin, C. reticulata, grapefruit or pomelo, C. paradisi, lemon, C. limon and lime, C. aurantifolia. The only other citrus species not in the genus Citrus that are grown commercially are kumquat, FortuneUa spp. and the trifoliate orange, Poncirus trifoliata, which is primarily produced for use as a rootstock. Citrus is grown in most of the tropical and subtropical areas of the World, with production restricted primarily by the regularity and severity of winter frost. Major commercial producers include Argentina, Australia, Brazil, China, Cuba, Egypt, India, Israel, Italy, Japan, Mexico, Morocco, South Africa, Spain and the United States (Ebeling, 1959; Snowdon, 1990; Whiteside, 1988). Most production is for the fresh fruit market, although the United States and Brazil produce processed, concentrated juices. World production of citrus varies from year to year but probably averages about 60 to 70 million tons (Rose, 1990; Snowdon, 1990; Whiteside, 1988). The 1991-1992 citrus crop (Anonymous, 1992) in the United States was estimated at 12.4 million tons for all varieties, with a value of 2.45 billion U.S. dollars. Present day commercial citrus varieties apparently all originated in the Far East. Movement of these varieties around the World has had a long and interesting history, much of which has been chronicled by Gallesio (1811), Tolkowsky (1938)and Webber (1967). The earliest known references to citrus are to be found in writings about the Chinese Emperor Ta Yu, who reigned from 2205 to 2197 B.C. The first citrus fruit recorded in the Middle East and Europe was the citron, Citrus medica. There is some archeological evidence that the citron was being raised in the Middle East by about 4000 B.C., although historically it was not mentioned as being present until after the reign of Alexander the Great in the late fourth century B.C. The first lemons and sour oranges are thought to have been present in the Mediterranean area by Roman times in the first and second centuries A.D, while the first sweet oranges to reach Europe are thought to have arrived in the early 15th century A.D. Many of the citrus varieties of that time were brought to the Americas by Columbus in 1493.
Section 3.3.1 references, p. 213
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Coccid pests of important crops
The Coccidae have been serious pests of citrus crops for well over one hundred years. With the advent of commercial plantings of citrus in California between 1860 and 1890, black scale, Saissetia oleae (Olivier), had become a pest of considerable importance. In 1911, H.J. Quayle and E.W. Rust wrote "The black scale, Saissetia oleae Bern, is widely distributed over most of the countries of the world, and has been known as a pest of the olive in the Old World nearly as far back as our entomological records go. Just when it was introduced into California, or from what country, doesn't appear to be established. The first complete account of its occurrence here is given in Comstock's report for 1880. It had been in the State, however, many years previous to that time. By 1880 it was well established in various parts of the State, and found infesting a wide range of food plants; but it was at that time, as now, a particularly serious enemy to citrus trees." With the influx of large numbers of settlers from the developing United States to the east following the "Gold Rush" of 1849, large citrus plantings were established rapidly. With their planting came a major complex of pest species, particularly in the Coccoidea. According to historical accounts, two of them, the California red scale, Aonidiella aurantii (Maskell) (Diaspididae) and the cottony cushion scale, Icerya purchasi Maskell (Margarodidae), were introduced into California by the 1870's, apparently directly from Australia. No one seems to know when black scale arrived in California. Since it was such a common problem on olive in the Mediterranean region from early times, it is not unreasonable to suspect that the scale may have been introduced into California on olive trees brought there by the Spaniards when they colonized upper and lower California and the surrounding areas in the mid-1700' s. Black scale was to become a pest of major importance on citrus in California and in other parts of the World, and it has remained a problem in many of them fight up to the present time. Although several species of Coccidae have been serious pests of citrus in various parts of the world and at various times, they are not generally considered to be the most serious scale insect pests of citrus (Ebeling, 1950). The armored scale insects (Diaspididae) are generally considered to be more economically important (Ebeling, 1950). Various species such as the California red scale, A. aurantii, the purple scale, Lepidosaphes beckii (Newman), the Florida red scale Chrysomphalus aonidum (Linnaeus) and others have caused major loses to citrus in the past. These armored scales are generally harder to control, are less influenced by natural enemies, are more prolific (usually with multiple generations per year), and have a more profound affect on the host (i.e. the California red scale is known to kill mature citrus trees if left unchecked for several years). Often, outbreaks of soft scales in citrus orchards have been shown to be related to control practices designed primarily for the control of the above diaspidids. The Coccidae normally cause direct injury to citrus by removing fluids and nutrient materials, primarily from the phloem, resulting in decreased vigor, with resultant loss in fruit quality and quantity. Soft scales feed primarily on the leaves and twigs of citrus. They are not known to feed on fruit. Soft scales also cause indirect injury to citrus by producing copious amounts of honeydew which in turn serves as a substrate for sooty moulds. A network of black sooty mould mycelia covers the leaf and fruit surfaces. In the case of the leaves, this mycelial cover is believed to block sunlight, resulting in loss of photosynthetic surfaces and thus reducing plant vigor (Quayle, 1911; see Section 1.2.2.2). A mycelial cover on the fruit causes it to be stained and dirty, and the mat-like, woven nature of the mycelia makes washing the fruit in the processing plant extremely difficult, causing a reduction in quality, grade and salability of the fruit. The black mats of sooty mould also act as a heat sink, causing the leaves and fruit to become too hot, eventually causing scorching.
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C/trus
SPECIES OF ECONOMIC IMPORTANCE The following is a summary (not in order of importance) of the more serious soft scale pests of citrus throughout the World. A summary of the status of biological control for most of the important species listed below will be found in Bartlett (1978).
Mediterranean Black Scale, Saissetia oleae (Olivier) This coccid is also called black scale in North America. It is the most serious soft scale pest of citrus on a world-wide basis. Some of its history on citrus crops is covered above. Black scale was to become a pest of major importance on citrus in California and was already causing over 2 million dollars loss annually by 1926 (Essig, 1926). Not until several effective parasitoids were introduced from South Africa in 1937 by Harold Compere did the seriousness of the black scale problem begin to abate somewhat. In as little as four years after the release of Metaphycus helvolus (Compere), only 0.5 percent of the citrus groves in Los Angeles had economically important populations of black scale (Ebeling, 1950). While black scale became a serious pest on citrus in California and on olives in the Mediterranean early in the developing history of Entomology, it is not necessarily a pest in all areas of California, nor in all other citrus growing areas of the World where it occurs. Black scale has two different populations in California, a single-brooded population that occurs in most of its geographical range, and a two-brooded population that occurs primarily in the cool coastal localities. In the early days, black scale was not considered a pest in the inland districts of California, such as the San Joaquin and Sacramento Valleys of central California, nor in the Riverside-Redlands citrus districts of southern California (Quayle, 1938). The limiting factor, apparently, was high summer temperatures of over 100~ (38~ which were lethal to the younger stages of the scale. Perhaps, for the same reason, black scale was primarily a problem in coastal locations in other countries, such as in Spain, Israel and New South Wales (Quayle, 1938). While South Africa has a climate very similar to that of California, black scale was never a problem there, apparently because of effective control by natural enemies. There are numerous species of Saissetia, including oleae, which are endemic to Africa, where effective parasitoids and predators for black scale occur naturally. According to Ebeling (1959), black scale rarely attacked citrus in Florida, even though it was common on other hosts. It was thought that black scale could not survive well on hosts other than its preferred olive or oleander if the climatic conditions were unfavorable to the scale. This would account for the low populations of black scale on citrus in the more inland and northern areas of California. As it was to turn out, however, a species complex of S. oleae was discovered. In the hot desert valleys of southeastern California, primarily in the Imperial Valley, entomologists and growers became aware of a strange phenomenon. Several citrus groves were surrounded by oleander (Nerium oleander) wind breaks which sustained an extremely heavy population of black scale but, even with the close proximity of these windbreaks to the citrus, the scale was never found in the groves. It was later noticed by entomologists from the University of California that the normal parasitoid species, which had been released to control the infestation, did not work on these scales (see Bartlett, 1960). Samples of the scale were sent to Howard McKenzie, then at the University of California, Davis, for identification, and he forwarded them to Giovanni De Lotto in South Africa. At about the same time, samples were also sent to De Lotto from Texas (Dean & Hart, 1972). At the time, De Lotto was working on the major soft scale groups in southern Africa, including the genera Coccus and Saissetia. After securing more material of Saissetia
Section 3.3.1 references, p. 213
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Coccid pests of important crops
from other parts of North America, De Lotto (197 lb) discovered that there were actually three species of black scales present in the United States, namely S. oleae, S. neglecta De Lotto and S. miranda (Cockerell & Parrott). It was found that S. neglecta was much more common in Florida than S. oleae, apparently because it is better adapted to the high humidities of the southeastern United States. In addition, S. neglecta apparently does not do well on citrus. Similarly, S. miranda prefers hosts other than citrus, particularly Nerium and Ficus, and is found in large numbers in the hot, dry, inland areas of Mexico and southeastern California, climatic areas that are unfavorable for S. oleae. Even though recorded from citrus in Texas (Dean and Hart, 1972), S. miranda has never become a problem on that host there. Black scale generally continues to be a problem in most coastal citrus growing areas of the world. Examples are the Middle East (Talhouk, 1969), Spain (Quayle, 1914, 1938; Ebeling, 1959; Moreno and Garijo, 1980), Sicily (Quayle, 1914; Viggiani, 1978) and, until just recently, Israel (Ben-Dov, 1988; Mendel et al., 1982, 1984; Podoler et al., 1979a, 1979b). In Israel, the importance of black scale had increased considerably in the 1970s (Blumberg and Swirski, 1988) but the introduction and management of several parasitoids, especially Metaphycus bartletti Annecke and Mynhardt, have been instrumental in controlling it there commercially. Rose (1990) has summarized the economic value of citrus production over the last 20 years. Actual assessment of losses caused by black scale or other Coccidae on citrus is not available on a world wide basis. However, in California it was still causing an estimated $1,049,146 per annum in the late 1970s, the last years for which such figures are available (Anonymous, 1978). The California loss and damage estimates included both direct losses, such as reduced yield, and indirect losses, such as from reduced fruit grades due to the stained appearance caused by sooty mould and to the cost of chemical controls. Economic losses from and control of black scale in California in the 1980's and 1990's has changed little from the situation in the 1970's except that more orchards are being brought under biological control, particularly for California red scale. Also, the acreage of citrus in the coastal areas of California is declining rapidly, so that less pesticides are being applied for black scale control in the state. This means that the effectiveness of natural enemies for black scale is increasing. An in-depth overview of biological control of black scale can be found in Bartlett (1978). Kennett (1979, 1986) reported on the importation and establishment in California of parasitoids in order to improve the control of the black scale. Brown soft scale, Coccus hesperidum Linnaeus Besides being probably the most abundant and wide-spread of all soft scale species, it is common and generally distributed in all citrus growing regions of the World. However, it rarely becomes a pest of economic importance to citrus, since a complex of parasitoids regulate its populations (Bartlett, 1978). It is present but of little concern in the citrus groves of the United States, Australia and the Mediterranean (Ebeling, 1959). In California, it is either controlled incidentally to California red scale control or is under effective biological control (Quayle, 1938; Ebeling, 1959; Bartlett, 1978) and outbreaks only periodically require chemical control. It has been a serious pest in the Middle East, South Africa (Stapley & Gayner, 1969) and Zimbabwe (Hodgson, 1970; Wilson and Goldsmid, 1962).
Citricola scale, Coccus pseudomagnoliarum (Kuwana) For many years it was known only from California, where it was occasionally a serious pest of citrus, primarily before the advent of modem insecticides (Gill, 1988). Since 1945, it has only been an occasional pest in California and usually only in isolated portions of affected groves. The effectiveness of the natural enemies of this species is well documented (Quayle, 1938; Bartlett, 1953, 1978; Gressit et al., 1954; Ebeling, 1959; On~iier, 1974). However, Elmer et al. (1980) stated that the complement of
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Citrus
natural enemies in the Central Valley of California would not be adequate to control citricola scale if chemical treatment for California red scale were to cease. Part of the problem is that citricola scale is highly susceptible to the chemical control measures for California red scale; in addition it is in the wrong life stage when the parasitoids for brown soft scale are active. In recent years it has been found in the Mediterranean (Barbagallo, 1974; Tranfaglia, 1974; Argyriou and Ioannides, 1975)and Middle Eastern regions (Onqiier, 1974; Onqiier and Tunqyureck, 1976; Talhouk, 1975). It is also a minor pest of citrus in Australia in the Riverina and Murray River districts (Beattie and Gellatley, 1983). Unlike the similar brown soft scale, it is a univoltine species. Red wax scale, Ceroplastes rubens (Maskell) It has been an important pest of citrus in Queensland, Australia, since before 1934 (Smith, 1976) and in Japan following its introduction there in 1897 (Yasumatsu, 1958). In Japan, it was considered to be a serious pest of citrus and about 150 other plants in the early part of the 20th century. Because of this, a parasitoid from Hawaii and California was released between 1932 and 1938, but without success. In 1946, Yasumatsu discovered the parasitoid Anicetus beneficus Ishii and Yasumatsu in the orchards of Kyushu Prefecture. This parasitoid was then released in other areas of Japan, including Honshu and Shikoku, and it quickly gave commercial control of the scale. It was also considered to be the dominant scale pest on citrus in Queensland by Smith (1976). Although particularly important near Howard, it is generally a pest in all the coastal and sub-coastal citrus growing areas. It produces copious honeydew and sooty mould and is, therefore, a big problem on the leaves and fruit. All varieties of fruit are attacked, but Beattie and Gellatley (1983) now consider it a major pest only on mandarins. Unlike some other wax scale species which are potential citrus pests but have only one annual generation, C. rubens has two. White wax scale, Ceroplastes destructor Newstead Has been troublesome in Australia in the coastal and northwestern citrus growing areas (Beattie and Gellatley, 1983), although it has declined in importance in recent years (Beatty, 1988; Hely et al., 1982; Milne, 1981). It is univoltine in most of Australia but occasionally produces a partial second generation in the warmer northwestern citrus growing areas (Beattie and Gellatley, 1983). Ceroplastes destructor is also listed as a pest in South Africa. Chinese wax scale, Ceroplastes sinensis Del Guercio In Australia, it was first found on citrus in 1966 (Snowball, 1970) and has since been displacing the other wax scale species as the most serious scale pest of citrus (Beatty, 1988). It occurs primarily in the coastal districts and is univoltine. Although this species requires chemical control in Australia, it is only a sporadic pest in other citrus growing areas, such as Spain and Italy (Gill, 1988). It is recorded from California, where populations are often high on the pepper tree (Schinus molle) and other hosts and, while the species is slowly expanding its range there, it still occurs only in suburban areas and has not reached the commercial citrus orchards. Florida wax scale, Ceroplastes floridensis Comstock Although probably present in Israel since the start of the 20th century (Ben-Dov, 1988), it only became an important pest of citrus in Israel on the introduction of organochlorine insecticides (Avidov & Harpaz, 1969). It is now generally kept below the economic threshold by reduced use of chemicals and an improved use of natural enemies (Peleg
Section 3.3.1 references, p. 213
Coccid pests of important crops
212
and Bar-Zakay, 1995). On the rare occasions that chemicals are now required, insect growth regulators (IGRs), such as buprofezin, are now recommended as they are highly efficient against the nymphal stages and young adults (Peleg, 1988).
Cottony citrus scale, Pulvinaria citricola K u w a n a Occurs in the U S A and Japan. It is a single brooded species that is occasionally serious on citrus in Shizuoka and Okayama, Japan (Quayle, 1938).
Tables of major and minor soft scale pests of citrus In Tables 3.3.1.1, 3.3.1.2 and 3.3.1.3 are listed the known soft scale species recorded from citrus and the general geographical areas were they are known to occur. The lists were compiled from Ebeling (1959), Talhouk (1975), Kamburov (1987), Ben-Dov (1988) and Schmutterer (1990).
TABLE 3.3.1.1 The major sot~ scale pests of citrus Species
Countries affected
Ceroplastes rubens OVlaskell) Coccus pseudomagnoliarum (Kuwana)
Australia, China, India, Japan. Australia, Indonesia, Japan, Mediterranean region, Russia, Tropical North America, USA (California). Australia, Caribbean, Israel, Japan, Mediterranean region, Russia, South America, Tropical North America, USA (California, Texas).
Saissetia oleae (Olivier)
TABLE 3.3.1.2 Minor sotI scale pests of citrus. Species
Countries affected
India, Japan, Tropical North America, USA (Florida). Australia, South Africa. Caribbean, China, India, Israel, Japan, Mediterranean region, Tropical North, America, USA (Florida). South America. Ceroplastes grandis Hempel Israel, Mediterranean region, Russia. Ceroplastes rusci Linnaeus Mediterranean region, Russia, South America. Ceroplastes sinensis Del Guercio Chloropulvinariafloccifera (Westwood) India, Mediterranean region, Russia. Chloropulvinariapsidii (Maskell) India, Indonesia, Philippines, Tropical North America, USA (Florida). Cribrolecanium andersoni (Newstead) South Africa. Australia, Caribbean, India, Israel, Japan, Mediterranean region, Coccus hesperidum Linnaeus Russia, South America, Tropical North America, USA, Zimbabwe. Caribbean, India, Indonesia, South America, Tropical North Coccus viridis (Green) America, USA (Florida), . Mesolecanium deltae (Lizer y Trelles) South America. India, Indonesia, Israel, Tropical North America, USA. Parasaissetia nigra (Nietner) Japan, Russia. Pulvinaria aurantii Cockerell Japan. Pulvinaria citricola Kuwana Australia, Malaysia, Philippines. Pulvinaria polygonata Cockerell India, Indonesia, Israel, South America, Tropical North America, Saissetia coffeae (Walker) USA. ToumeyeUa cubensis Heidel & K6hler Cuba, Puerto Rico. Ceroplastes ceriferus (Fabricius) Ceroplastes destructor (Newstead) Ceroplastes floridensis Comstock
C/trus
213 TABLE 3.3.1.3 Sot~ scales recordes from citrus, which are of little or no importance. Species
Countries affected
Ceroplastes actiniformis Green Ceroplastes bergi Cockerell Ceroplastes cirripediformis Comstock Coccus africanus Newstead Coccus bicruciatus (Green) Coccus capparidis (Green) Coccus discrepans (Green) Coccus longulus (Douglas) Coccus watti (Green) Mallococcus lanigerus (Hempel) Mesolecanium nigrofasciatum (Pergande) Milviscutulus mangiferae (Green) Paralecanium expansum (Green) Protopulvinaria pyriformis Cockerell Pulvinaria ceUulosa Green Pulvinaria ficus Hempel Pulvinaria flavescens Brethes Pulvinaria horii Kuwana Pulvinaria japonica (Kuwana) Pulvinaria mammeae Maskell Pulvinaria okitsuensis Kuwana Pulvinaria ornata Froggatt Pulvinaria peninsularis Ferris Pulvinaria thespesiae Green Pulvinaria urbicola Cockerell Pulvinaria vitis (Linnaeus) Vinsonia stellifera Westwood
India. Brazil. South America, Tropical North America, USA. South Africa. India. Israel. India. Israel, Philippines. Malaysia. Brazil. USA (Florida). India, Israel, USA. Australia. Mediterranean region, Tropical North America, USA (Florida). Asia, India. Brazil. Brazil. Russia. Japan. Hawaii. Japan. Australia. Mexico. India. Tropical North America, USA (Florida). USA. Pakistan.
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Dean, H.A. and Hart, W.G., 1972. Saissetia miranda (Homoptera: Coccidae), a potential pest of Citrus in Texas. Annals of the Entomological Society of America, 65(2): 478-481. De Lotto, G., 1971a. The authorship of the Mediterranean black scale (Homoptera: Coccidae). Journal of Entomology (B), 40(2): 149-150. De Lotto, G., 1971b. A preliminary note on the black scales (Homoptera: Coccidae) of North and Central America. Bulletin of Entomological Research, 81" 325-326. Ebeling, W., 1950. Subtropical Entomology. Lithotype Process Co., San Francisco. 747 pp. Ebeling, W., 1959. Subtropical Fruit Pests. University of California Division of Agriculture Science, Los Angeles. 436 pp. Elmer, H.S., Brawner, O.L. and Ewart, W.E., 1980. California red scale predator may create citricola scale dilemma. California Agriculture, 34(11-12): 20-21. Essig, E.O., 1926. Insects of Western North America. The Macmillan Co., New York. 1036 pp. Gallesio, G., 1811. Traite du Citrus. Louis Fantin, Paris. 381 pp. Gill, R.J., 1988. The Scale Insects of California. Part 1: The Soft Scales. California Department of Food & Agriculture Technical Series in Agricultural Biosystematics and Plant Pathology, 1:1-132. Gressitt, J.L., Flanders J.E. and Bartlett, B., 1954. Parasites of citricola scale in Japan, and their introduction into California. Pan-Pacific Entomologist, 30(1): 5-9. Hely, P.C., Pasfield, G. and Gellatley, J.G. 1982. Insect Pests of Fruit and Vegetables in New South Wales. Inkata Press: Melbourne. 312 pp Hodgson, C.J., 1970. Pests of citrus and their control. PANS, Tropical Pesticides Research Headquarters & Information Unit, 16(4): 647-666. Kamburov, S.S., 1987. New pests and beneficial insects on citrus in South Africa. Citrus & Subtropical Fruit Journal, 636: 19-20. Kennett, C.E., 1979. Occurrence of Metaphycus bartletti Annecke and Mynhardt, a South Africa parasite of black scale, Saissetia oleae (Olivier) in central and northern California. Pan-Pacific Entomologist, 56: 107-110. Kennett, C.E., 1986. A survey of the parasitoid complex attacking black scale, Saissetia oleae (Olivier), in central and northern California (Hymenoptera: Chalcidoidea; Homoptera: Coccidae). Pan-Pacific Entomologist, 62: 363-369. Mendel, Z., Podoler, H. and Rosen, D., 1982. Population dynamics of the Mediterranean black scale, Saissetia oleae (Oliv.), on citrus in Israel. 3. Occurence of a yellow form. Journal of the Entomological Society of Southern Africa, 45: 227-229. Mendel, Z., Podoler, H. and Rosen, D., 1984. Population dynamics of the Mediterranean black scale, Saisseu'a oleae (Oliv.), on citrus in Israel. 5. The crawlers. Journal of the Entomological Society of Southern Africa, 47: 23-34. Milne, W.M., 1981. Insecticidal versus natural control of white wax scale (Gascardia destructor) at Kenthurst N.S.W., during 1972-73. Journal of the Australian Entomological Society, 20:167-170. Moreno, R and Garijo, C., 1980. Dinamica de poblaciones de Saissetia oleae Oliv. (Hom., Coccidae) sobre citricos. Comparacion de diversos metodos para estimar la densidad de adultos a nivel de arbol. Boletfn del Servicio de Defensa contra Plagas e Inspecci6n Fitopathal6gica, 6(1): 75-94. On~iier, C., 1974. The Coccus species (Homoptera:Coccidae) damaging Citrus groves in the Aegean region; studies on their morphological characters, distribution and natural enemies. Bitki Koruma Bulletin Supplement, 1: 1-59. [Abstracted in Review of Applied Entomology 64(3): 433.] On~iier, C. and Tun~yureck, M., 1976. Observations on the biology and natural enemies of Coccus pseudomagnoliarum Kuw. in Citrus orchards in the Aegean Region. Bulletin SROP 5:255-257. [Abstracted in Review of Applied Entomology 64(10): 1706.] Peleg, B.A., 1988. Effect of a new phenoxy juvenile hormone analog on California red scale (Homoptera: Diaspididae), Florida wax scale (Homoptera: Coccidae) and the ectoparasite Aphytis holoxantus DeBach (Hymenoptera: Aphelinidae). Journal of Economic Entomology, 8: 88-92. Peleg, B.A. and Bar-Zakay, I., 1995. The pest status of citrus scale insects in Israel (1984-1994). Israel Journal of Entomology, 29: 261-264. Podoler, H., Bar-Zacay, I. and Rosen, D., 1979a. Population dynamics of the Mediterranean black scale, Saissetia oleae (Olivier), on citrus in Israel. 1. A partial life table. Journal of the Entomological Society of Southern Africa, 42(2): 257-266. Podoler, H., Bar-Zacay, I. and Rosen, D., 1979b. Population dynamics of the Mediterranean black scale, Saissetia oleae (Olivier), on citrus in Israel. II. Distribution within the citrus tree. Journal of the Entomological Society of Southern Africa, 42(2)" 267-273. Quayle, H.J., 1911. Citrus fruit insects. California Agricultural Experiment Station Bulletin, 214:445-512. Quayle, H.J., 1914. Citrus fruit insects in the Mediterranean countries. Bulletin of the United States Department of Agriculture, 134: 1-35. Quayle, H.J., 1938. Insects of Citrus and Other Subtropical Fruits. Comstock Publishing Company, Ithaca, New York. 583 pp. Quayle, H.J. and Rust, E.W., 1911. The black scale, Saissetia oleae Bern. California Agricultural Experiment Station Bulletin, 223:151-200.
Citrus
215 Rose, M., 1990. Diaspidid pest problems and control in crops: Citrus. In: D. Rosen (Editor), World Crop Pests: Armored Scale Insects - Their Biology, Natural Enemies and Control. Volume 4b. Elsevier, Amsterdam. pp. 535-541. Schmutterer, H., 1990. Crop Pests in the Caribbean with Particular Reference to the Dominican Republic. Deutsche Gesellshat~ fiir Technische Zusammerarbeit (GTZ) GmbH, Eshborn, Germany. 640 pp. Smith, D., 1976. The seasonal history and control of Ceroplastes rubens Maskell on citrus in south-east Queensland. Queensland Journal of Agricultural and Animal Sciences, 33(1): 23-30. Snowball, G.J., 1970. Ceroplastes sinensis Del Guercio (Homoptera: Coccidae). Journal of the Australian Entomological Society, 9: 57-66. Snowdon, A.L., 1990. A Color Atlas of Post-harvest Diseases and Disorders of Fruits and Vegetables. Volume 1: General Introduction and Fruits. CRC Press, Inc., Bocas Raton, Florida, U.S.A. 302 pp. Stapley, J.H. and Gaynor, F.C.H., 1969. World Crop Protection, Volume 1: Posts and Diseases. Iife Books Limited, England and Chemical Rubber Co., Cleveland, Ohio. 270 pp. Talhouk, A.S., 1969. Insects and Mites Injurious to Crops in Middle Eastern Countries. Monographien zur angewandten Entomologie, 21: 1-239. Talhouk, A.S., 1975. Citrus pests throughout the world. Ciba-Geigy Agrochemicals, Technical Monograph, 4: 1-88. Tolkowsky, S. 1938. Hesperides. A History of the Culture and Use of Citrus Fruits. John Bole, Sons and Curnow, London. 371 pp. Tranfaglia, A., 1974. Studi sugli Homoptera Coccoidea. Ill. Un nuovo Coccino (Coccus aegaeus De Lotto) sugli Agrumi in Italia (notizae preliminari). Bolletino del Laboratorio di Entomologia Agraria "Filippo Silvestri" Portici, 35: 141-144. Viggiani, G., 1978. Current state of biological control of olive scales. Bolletino dol Laboratorio di Entomologia Agraria "Filippo Silvestri" Portici, 35: 30-38. Webber, H.J., 1967. History and development of the citrus industry. In: The Citrus Industry. Vol. I. History, World Distribution, Botany and Varieties (Revised by W. Reuther and H.W. Lawton). A Centennial Publication. University of California Press, Berkeley, pp. 1-39. Whitesido, J.O., 1988. Introduction, citrus trees and their fruit. In: J.O. Whiteside, S.M. Garnsey, and L.W. Timmor (Editors), Compendium of citrus diseases. APS Press (American Pathological Society), St. Paul, Minnesota. 80 pp. Wilson, K. and Goldsmid, J.M., 1962. Rhodesian citrus pests and their control. Rhodesian Agricultural Journal (Bulletin No. 2127), 59: 41-61. Yasumatsu, K., 1958. An interesting case of biological control of Ceroplastes rubens Maskell in Japan. Proceedings Tenth International Congress of Entomology (1956), 4: 771-775.
Chapter 3.3 Crops 3.3.1
207
Coccid Pests of Important
Citrus
RAYMOND J. GILL
INTRODUCTION The citrus fruit, because of its attractiveness, good taste and nutritive value, has gained popularity with peoples all over the globe. Trees of certain Citrus varieties are attractive in their own fight and have been used in ornamental landscaping. The leaves of particular varieties are used as a spice, particularly with chicken dishes and, in some cultures, the rind is used medicinally. The major commercial citrus species that are currently being grown (Snowdon, 1990; Whiteside, 1988) include sweet orange, Citrus sinensis, mandarin, C. reticulata, grapefruit or pomelo, C. paradisi, lemon, C. limon and lime, C. aurantifolia. The only other citrus species not in the genus Citrus that are grown commercially are kumquat, FortuneUa spp. and the trifoliate orange, Poncirus trifoliata, which is primarily produced for use as a rootstock. Citrus is grown in most of the tropical and subtropical areas of the World, with production restricted primarily by the regularity and severity of winter frost. Major commercial producers include Argentina, Australia, Brazil, China, Cuba, Egypt, India, Israel, Italy, Japan, Mexico, Morocco, South Africa, Spain and the United States (Ebeling, 1959; Snowdon, 1990; Whiteside, 1988). Most production is for the fresh fruit market, although the United States and Brazil produce processed, concentrated juices. World production of citrus varies from year to year but probably averages about 60 to 70 million tons (Rose, 1990; Snowdon, 1990; Whiteside, 1988). The 1991-1992 citrus crop (Anonymous, 1992) in the United States was estimated at 12.4 million tons for all varieties, with a value of 2.45 billion U.S. dollars. Present day commercial citrus varieties apparently all originated in the Far East. Movement of these varieties around the World has had a long and interesting history, much of which has been chronicled by Gallesio (1811), Tolkowsky (1938)and Webber (1967). The earliest known references to citrus are to be found in writings about the Chinese Emperor Ta Yu, who reigned from 2205 to 2197 B.C. The first citrus fruit recorded in the Middle East and Europe was the citron, Citrus medica. There is some archeological evidence that the citron was being raised in the Middle East by about 4000 B.C., although historically it was not mentioned as being present until after the reign of Alexander the Great in the late fourth century B.C. The first lemons and sour oranges are thought to have been present in the Mediterranean area by Roman times in the first and second centuries A.D, while the first sweet oranges to reach Europe are thought to have arrived in the early 15th century A.D. Many of the citrus varieties of that time were brought to the Americas by Columbus in 1493.
Section 3.3.1 references, p. 213
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Coccid pests of important crops
The Coccidae have been serious pests of citrus crops for well over one hundred years. With the advent of commercial plantings of citrus in California between 1860 and 1890, black scale, Saissetia oleae (Olivier), had become a pest of considerable importance. In 1911, H.J. Quayle and E.W. Rust wrote "The black scale, Saissetia oleae Bern, is widely distributed over most of the countries of the world, and has been known as a pest of the olive in the Old World nearly as far back as our entomological records go. Just when it was introduced into California, or from what country, doesn't appear to be established. The first complete account of its occurrence here is given in Comstock's report for 1880. It had been in the State, however, many years previous to that time. By 1880 it was well established in various parts of the State, and found infesting a wide range of food plants; but it was at that time, as now, a particularly serious enemy to citrus trees." With the influx of large numbers of settlers from the developing United States to the east following the "Gold Rush" of 1849, large citrus plantings were established rapidly. With their planting came a major complex of pest species, particularly in the Coccoidea. According to historical accounts, two of them, the California red scale, Aonidiella aurantii (Maskell) (Diaspididae) and the cottony cushion scale, Icerya purchasi Maskell (Margarodidae), were introduced into California by the 1870's, apparently directly from Australia. No one seems to know when black scale arrived in California. Since it was such a common problem on olive in the Mediterranean region from early times, it is not unreasonable to suspect that the scale may have been introduced into California on olive trees brought there by the Spaniards when they colonized upper and lower California and the surrounding areas in the mid-1700' s. Black scale was to become a pest of major importance on citrus in California and in other parts of the World, and it has remained a problem in many of them fight up to the present time. Although several species of Coccidae have been serious pests of citrus in various parts of the world and at various times, they are not generally considered to be the most serious scale insect pests of citrus (Ebeling, 1950). The armored scale insects (Diaspididae) are generally considered to be more economically important (Ebeling, 1950). Various species such as the California red scale, A. aurantii, the purple scale, Lepidosaphes beckii (Newman), the Florida red scale Chrysomphalus aonidum (Linnaeus) and others have caused major loses to citrus in the past. These armored scales are generally harder to control, are less influenced by natural enemies, are more prolific (usually with multiple generations per year), and have a more profound affect on the host (i.e. the California red scale is known to kill mature citrus trees if left unchecked for several years). Often, outbreaks of soft scales in citrus orchards have been shown to be related to control practices designed primarily for the control of the above diaspidids. The Coccidae normally cause direct injury to citrus by removing fluids and nutrient materials, primarily from the phloem, resulting in decreased vigor, with resultant loss in fruit quality and quantity. Soft scales feed primarily on the leaves and twigs of citrus. They are not known to feed on fruit. Soft scales also cause indirect injury to citrus by producing copious amounts of honeydew which in turn serves as a substrate for sooty moulds. A network of black sooty mould mycelia covers the leaf and fruit surfaces. In the case of the leaves, this mycelial cover is believed to block sunlight, resulting in loss of photosynthetic surfaces and thus reducing plant vigor (Quayle, 1911; see Section 1.2.2.2). A mycelial cover on the fruit causes it to be stained and dirty, and the mat-like, woven nature of the mycelia makes washing the fruit in the processing plant extremely difficult, causing a reduction in quality, grade and salability of the fruit. The black mats of sooty mould also act as a heat sink, causing the leaves and fruit to become too hot, eventually causing scorching.
209
C/trus
SPECIES OF ECONOMIC IMPORTANCE The following is a summary (not in order of importance) of the more serious soft scale pests of citrus throughout the World. A summary of the status of biological control for most of the important species listed below will be found in Bartlett (1978).
Mediterranean Black Scale, Saissetia oleae (Olivier) This coccid is also called black scale in North America. It is the most serious soft scale pest of citrus on a world-wide basis. Some of its history on citrus crops is covered above. Black scale was to become a pest of major importance on citrus in California and was already causing over 2 million dollars loss annually by 1926 (Essig, 1926). Not until several effective parasitoids were introduced from South Africa in 1937 by Harold Compere did the seriousness of the black scale problem begin to abate somewhat. In as little as four years after the release of Metaphycus helvolus (Compere), only 0.5 percent of the citrus groves in Los Angeles had economically important populations of black scale (Ebeling, 1950). While black scale became a serious pest on citrus in California and on olives in the Mediterranean early in the developing history of Entomology, it is not necessarily a pest in all areas of California, nor in all other citrus growing areas of the World where it occurs. Black scale has two different populations in California, a single-brooded population that occurs in most of its geographical range, and a two-brooded population that occurs primarily in the cool coastal localities. In the early days, black scale was not considered a pest in the inland districts of California, such as the San Joaquin and Sacramento Valleys of central California, nor in the Riverside-Redlands citrus districts of southern California (Quayle, 1938). The limiting factor, apparently, was high summer temperatures of over 100~ (38~ which were lethal to the younger stages of the scale. Perhaps, for the same reason, black scale was primarily a problem in coastal locations in other countries, such as in Spain, Israel and New South Wales (Quayle, 1938). While South Africa has a climate very similar to that of California, black scale was never a problem there, apparently because of effective control by natural enemies. There are numerous species of Saissetia, including oleae, which are endemic to Africa, where effective parasitoids and predators for black scale occur naturally. According to Ebeling (1959), black scale rarely attacked citrus in Florida, even though it was common on other hosts. It was thought that black scale could not survive well on hosts other than its preferred olive or oleander if the climatic conditions were unfavorable to the scale. This would account for the low populations of black scale on citrus in the more inland and northern areas of California. As it was to turn out, however, a species complex of S. oleae was discovered. In the hot desert valleys of southeastern California, primarily in the Imperial Valley, entomologists and growers became aware of a strange phenomenon. Several citrus groves were surrounded by oleander (Nerium oleander) wind breaks which sustained an extremely heavy population of black scale but, even with the close proximity of these windbreaks to the citrus, the scale was never found in the groves. It was later noticed by entomologists from the University of California that the normal parasitoid species, which had been released to control the infestation, did not work on these scales (see Bartlett, 1960). Samples of the scale were sent to Howard McKenzie, then at the University of California, Davis, for identification, and he forwarded them to Giovanni De Lotto in South Africa. At about the same time, samples were also sent to De Lotto from Texas (Dean & Hart, 1972). At the time, De Lotto was working on the major soft scale groups in southern Africa, including the genera Coccus and Saissetia. After securing more material of Saissetia
Section 3.3.1 references, p. 213
210
Coccid pests of important crops
from other parts of North America, De Lotto (197 lb) discovered that there were actually three species of black scales present in the United States, namely S. oleae, S. neglecta De Lotto and S. miranda (Cockerell & Parrott). It was found that S. neglecta was much more common in Florida than S. oleae, apparently because it is better adapted to the high humidities of the southeastern United States. In addition, S. neglecta apparently does not do well on citrus. Similarly, S. miranda prefers hosts other than citrus, particularly Nerium and Ficus, and is found in large numbers in the hot, dry, inland areas of Mexico and southeastern California, climatic areas that are unfavorable for S. oleae. Even though recorded from citrus in Texas (Dean and Hart, 1972), S. miranda has never become a problem on that host there. Black scale generally continues to be a problem in most coastal citrus growing areas of the world. Examples are the Middle East (Talhouk, 1969), Spain (Quayle, 1914, 1938; Ebeling, 1959; Moreno and Garijo, 1980), Sicily (Quayle, 1914; Viggiani, 1978) and, until just recently, Israel (Ben-Dov, 1988; Mendel et al., 1982, 1984; Podoler et al., 1979a, 1979b). In Israel, the importance of black scale had increased considerably in the 1970s (Blumberg and Swirski, 1988) but the introduction and management of several parasitoids, especially Metaphycus bartletti Annecke and Mynhardt, have been instrumental in controlling it there commercially. Rose (1990) has summarized the economic value of citrus production over the last 20 years. Actual assessment of losses caused by black scale or other Coccidae on citrus is not available on a world wide basis. However, in California it was still causing an estimated $1,049,146 per annum in the late 1970s, the last years for which such figures are available (Anonymous, 1978). The California loss and damage estimates included both direct losses, such as reduced yield, and indirect losses, such as from reduced fruit grades due to the stained appearance caused by sooty mould and to the cost of chemical controls. Economic losses from and control of black scale in California in the 1980's and 1990's has changed little from the situation in the 1970's except that more orchards are being brought under biological control, particularly for California red scale. Also, the acreage of citrus in the coastal areas of California is declining rapidly, so that less pesticides are being applied for black scale control in the state. This means that the effectiveness of natural enemies for black scale is increasing. An in-depth overview of biological control of black scale can be found in Bartlett (1978). Kennett (1979, 1986) reported on the importation and establishment in California of parasitoids in order to improve the control of the black scale. Brown soft scale, Coccus hesperidum Linnaeus Besides being probably the most abundant and wide-spread of all soft scale species, it is common and generally distributed in all citrus growing regions of the World. However, it rarely becomes a pest of economic importance to citrus, since a complex of parasitoids regulate its populations (Bartlett, 1978). It is present but of little concern in the citrus groves of the United States, Australia and the Mediterranean (Ebeling, 1959). In California, it is either controlled incidentally to California red scale control or is under effective biological control (Quayle, 1938; Ebeling, 1959; Bartlett, 1978) and outbreaks only periodically require chemical control. It has been a serious pest in the Middle East, South Africa (Stapley & Gayner, 1969) and Zimbabwe (Hodgson, 1970; Wilson and Goldsmid, 1962).
Citricola scale, Coccus pseudomagnoliarum (Kuwana) For many years it was known only from California, where it was occasionally a serious pest of citrus, primarily before the advent of modem insecticides (Gill, 1988). Since 1945, it has only been an occasional pest in California and usually only in isolated portions of affected groves. The effectiveness of the natural enemies of this species is well documented (Quayle, 1938; Bartlett, 1953, 1978; Gressit et al., 1954; Ebeling, 1959; On~iier, 1974). However, Elmer et al. (1980) stated that the complement of
211
Citrus
natural enemies in the Central Valley of California would not be adequate to control citricola scale if chemical treatment for California red scale were to cease. Part of the problem is that citricola scale is highly susceptible to the chemical control measures for California red scale; in addition it is in the wrong life stage when the parasitoids for brown soft scale are active. In recent years it has been found in the Mediterranean (Barbagallo, 1974; Tranfaglia, 1974; Argyriou and Ioannides, 1975)and Middle Eastern regions (Onqiier, 1974; Onqiier and Tunqyureck, 1976; Talhouk, 1975). It is also a minor pest of citrus in Australia in the Riverina and Murray River districts (Beattie and Gellatley, 1983). Unlike the similar brown soft scale, it is a univoltine species. Red wax scale, Ceroplastes rubens (Maskell) It has been an important pest of citrus in Queensland, Australia, since before 1934 (Smith, 1976) and in Japan following its introduction there in 1897 (Yasumatsu, 1958). In Japan, it was considered to be a serious pest of citrus and about 150 other plants in the early part of the 20th century. Because of this, a parasitoid from Hawaii and California was released between 1932 and 1938, but without success. In 1946, Yasumatsu discovered the parasitoid Anicetus beneficus Ishii and Yasumatsu in the orchards of Kyushu Prefecture. This parasitoid was then released in other areas of Japan, including Honshu and Shikoku, and it quickly gave commercial control of the scale. It was also considered to be the dominant scale pest on citrus in Queensland by Smith (1976). Although particularly important near Howard, it is generally a pest in all the coastal and sub-coastal citrus growing areas. It produces copious honeydew and sooty mould and is, therefore, a big problem on the leaves and fruit. All varieties of fruit are attacked, but Beattie and Gellatley (1983) now consider it a major pest only on mandarins. Unlike some other wax scale species which are potential citrus pests but have only one annual generation, C. rubens has two. White wax scale, Ceroplastes destructor Newstead Has been troublesome in Australia in the coastal and northwestern citrus growing areas (Beattie and Gellatley, 1983), although it has declined in importance in recent years (Beatty, 1988; Hely et al., 1982; Milne, 1981). It is univoltine in most of Australia but occasionally produces a partial second generation in the warmer northwestern citrus growing areas (Beattie and Gellatley, 1983). Ceroplastes destructor is also listed as a pest in South Africa. Chinese wax scale, Ceroplastes sinensis Del Guercio In Australia, it was first found on citrus in 1966 (Snowball, 1970) and has since been displacing the other wax scale species as the most serious scale pest of citrus (Beatty, 1988). It occurs primarily in the coastal districts and is univoltine. Although this species requires chemical control in Australia, it is only a sporadic pest in other citrus growing areas, such as Spain and Italy (Gill, 1988). It is recorded from California, where populations are often high on the pepper tree (Schinus molle) and other hosts and, while the species is slowly expanding its range there, it still occurs only in suburban areas and has not reached the commercial citrus orchards. Florida wax scale, Ceroplastes floridensis Comstock Although probably present in Israel since the start of the 20th century (Ben-Dov, 1988), it only became an important pest of citrus in Israel on the introduction of organochlorine insecticides (Avidov & Harpaz, 1969). It is now generally kept below the economic threshold by reduced use of chemicals and an improved use of natural enemies (Peleg
Section 3.3.1 references, p. 213
Coccid pests of important crops
212
and Bar-Zakay, 1995). On the rare occasions that chemicals are now required, insect growth regulators (IGRs), such as buprofezin, are now recommended as they are highly efficient against the nymphal stages and young adults (Peleg, 1988).
Cottony citrus scale, Pulvinaria citricola K u w a n a Occurs in the U S A and Japan. It is a single brooded species that is occasionally serious on citrus in Shizuoka and Okayama, Japan (Quayle, 1938).
Tables of major and minor soft scale pests of citrus In Tables 3.3.1.1, 3.3.1.2 and 3.3.1.3 are listed the known soft scale species recorded from citrus and the general geographical areas were they are known to occur. The lists were compiled from Ebeling (1959), Talhouk (1975), Kamburov (1987), Ben-Dov (1988) and Schmutterer (1990).
TABLE 3.3.1.1 The major sot~ scale pests of citrus Species
Countries affected
Ceroplastes rubens OVlaskell) Coccus pseudomagnoliarum (Kuwana)
Australia, China, India, Japan. Australia, Indonesia, Japan, Mediterranean region, Russia, Tropical North America, USA (California). Australia, Caribbean, Israel, Japan, Mediterranean region, Russia, South America, Tropical North America, USA (California, Texas).
Saissetia oleae (Olivier)
TABLE 3.3.1.2 Minor sotI scale pests of citrus. Species
Countries affected
India, Japan, Tropical North America, USA (Florida). Australia, South Africa. Caribbean, China, India, Israel, Japan, Mediterranean region, Tropical North, America, USA (Florida). South America. Ceroplastes grandis Hempel Israel, Mediterranean region, Russia. Ceroplastes rusci Linnaeus Mediterranean region, Russia, South America. Ceroplastes sinensis Del Guercio Chloropulvinariafloccifera (Westwood) India, Mediterranean region, Russia. Chloropulvinariapsidii (Maskell) India, Indonesia, Philippines, Tropical North America, USA (Florida). Cribrolecanium andersoni (Newstead) South Africa. Australia, Caribbean, India, Israel, Japan, Mediterranean region, Coccus hesperidum Linnaeus Russia, South America, Tropical North America, USA, Zimbabwe. Caribbean, India, Indonesia, South America, Tropical North Coccus viridis (Green) America, USA (Florida), . Mesolecanium deltae (Lizer y Trelles) South America. India, Indonesia, Israel, Tropical North America, USA. Parasaissetia nigra (Nietner) Japan, Russia. Pulvinaria aurantii Cockerell Japan. Pulvinaria citricola Kuwana Australia, Malaysia, Philippines. Pulvinaria polygonata Cockerell India, Indonesia, Israel, South America, Tropical North America, Saissetia coffeae (Walker) USA. ToumeyeUa cubensis Heidel & K6hler Cuba, Puerto Rico. Ceroplastes ceriferus (Fabricius) Ceroplastes destructor (Newstead) Ceroplastes floridensis Comstock
C/trus
213 TABLE 3.3.1.3 Sot~ scales recordes from citrus, which are of little or no importance. Species
Countries affected
Ceroplastes actiniformis Green Ceroplastes bergi Cockerell Ceroplastes cirripediformis Comstock Coccus africanus Newstead Coccus bicruciatus (Green) Coccus capparidis (Green) Coccus discrepans (Green) Coccus longulus (Douglas) Coccus watti (Green) Mallococcus lanigerus (Hempel) Mesolecanium nigrofasciatum (Pergande) Milviscutulus mangiferae (Green) Paralecanium expansum (Green) Protopulvinaria pyriformis Cockerell Pulvinaria ceUulosa Green Pulvinaria ficus Hempel Pulvinaria flavescens Brethes Pulvinaria horii Kuwana Pulvinaria japonica (Kuwana) Pulvinaria mammeae Maskell Pulvinaria okitsuensis Kuwana Pulvinaria ornata Froggatt Pulvinaria peninsularis Ferris Pulvinaria thespesiae Green Pulvinaria urbicola Cockerell Pulvinaria vitis (Linnaeus) Vinsonia stellifera Westwood
India. Brazil. South America, Tropical North America, USA. South Africa. India. Israel. India. Israel, Philippines. Malaysia. Brazil. USA (Florida). India, Israel, USA. Australia. Mediterranean region, Tropical North America, USA (Florida). Asia, India. Brazil. Brazil. Russia. Japan. Hawaii. Japan. Australia. Mexico. India. Tropical North America, USA (Florida). USA. Pakistan.
REFERENCES Anonymous, 1978. Estimated damage and crop loss caused by insect and mite pests, 1978. California Department of Food and Agriculture, Sacramento California, pp. 1-28. Anonymous, 1992. Citrus fruits 1992 summary. United States Department of Agriculture, National Agricultural Statistics Service, Agricultural Statistics Board Fr Nt, 3-1 (92), 14 pp. Argyriou, L.C. and Ioannides, A.G., 1975. Coccus aegaeus (Homoptera, Coccoidea, Coccidae) De Lotto: nouvelle esp~ce de 16canine de Citrus en Gr6ce. Fruits, 30: 161-162. Avidov, Z. and Harpaz, I., 1969. Plant Pests of Israel. Israel University Press, Jerusalem, 549 pp. Barbagallo, S., 1974. Notizie sulla presenza in Sicilia di una nuova Cocciniglia degli agrumi. Osservazioni biologiche preliminari. Entomologica, 10: 121-139. Bartlett, B.R., 1953. Natural control of citricola scale in California. Journal of Economic Entomology 46: 25-28. Bartlett, B.R., 1960. Biological races of the black scale, Saissetia oleae, and their specific parasites. Annals of the Entomological Society of America, 53: 383-385. Bartlett, B.R., 1978. Coccidae. pp. 5%74. In: C.P. Clausen (Editor), Introduced Parasites and Predators of Arthropod Pests and Weeds: a World Review. United States Department of Agriculture, Agricultural Handbook, 480: 1-545. Beattie, G.A.C., 1988. Life tables and biological control of white wax scale, Gascardia destructor (Newstead), and Chinese wax scale, Ceroplastes sinensis Del Guercio (Hemiptera: Coccidae). Proceedings of the XCVRI International Congress of Entomology, Vancouver, Washington, p. 384. Beattie, G.A.C. and Gellatley, J.G., 1983. Citrus scale insects. New South Wales Department of Agriculture Agfact H2. AE. 2, 6 pp. Ben-Dov, Y., 1988. The scale insects (Homoptera: Coccoidea) of citrus in Israel: diversity and pest status. Proceedings of the Sixth International Citrus Congress: Tel Aviv, Israel, 1988, R. Goren and K. Mendel (Editors), Balaban Publishers, Philadelphia/Rehovot, pp. I075-1082. Blumberg, D. and Swirski, E., 1988. Colonization ofMetaphycus spp. (Hymenoptera: Encyrtidae) for control of the Mediterranean black scale, Saissetia oleae (Olivier) (Homoptera: Coccidae) in Israel. Proceedings of the Sixth International Citrus Congress: Tel Aviv, Israel, 1988, R. Goren and K. Mendel (Editors), Balaban Publishers, Philadelphia/Rehovot, pp. 1209-1213.
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Dean, H.A. and Hart, W.G., 1972. Saissetia miranda (Homoptera: Coccidae), a potential pest of Citrus in Texas. Annals of the Entomological Society of America, 65(2): 478-481. De Lotto, G., 1971a. The authorship of the Mediterranean black scale (Homoptera: Coccidae). Journal of Entomology (B), 40(2): 149-150. De Lotto, G., 1971b. A preliminary note on the black scales (Homoptera: Coccidae) of North and Central America. Bulletin of Entomological Research, 81" 325-326. Ebeling, W., 1950. Subtropical Entomology. Lithotype Process Co., San Francisco. 747 pp. Ebeling, W., 1959. Subtropical Fruit Pests. University of California Division of Agriculture Science, Los Angeles. 436 pp. Elmer, H.S., Brawner, O.L. and Ewart, W.E., 1980. California red scale predator may create citricola scale dilemma. California Agriculture, 34(11-12): 20-21. Essig, E.O., 1926. Insects of Western North America. The Macmillan Co., New York. 1036 pp. Gallesio, G., 1811. Traite du Citrus. Louis Fantin, Paris. 381 pp. Gill, R.J., 1988. The Scale Insects of California. Part 1: The Soft Scales. California Department of Food & Agriculture Technical Series in Agricultural Biosystematics and Plant Pathology, 1:1-132. Gressitt, J.L., Flanders J.E. and Bartlett, B., 1954. Parasites of citricola scale in Japan, and their introduction into California. Pan-Pacific Entomologist, 30(1): 5-9. Hely, P.C., Pasfield, G. and Gellatley, J.G. 1982. Insect Pests of Fruit and Vegetables in New South Wales. Inkata Press: Melbourne. 312 pp Hodgson, C.J., 1970. Pests of citrus and their control. PANS, Tropical Pesticides Research Headquarters & Information Unit, 16(4): 647-666. Kamburov, S.S., 1987. New pests and beneficial insects on citrus in South Africa. Citrus & Subtropical Fruit Journal, 636: 19-20. Kennett, C.E., 1979. Occurrence of Metaphycus bartletti Annecke and Mynhardt, a South Africa parasite of black scale, Saissetia oleae (Olivier) in central and northern California. 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