Tenuipalpidae, Berlese, 1913

Vacante, V., 2010, REVIEW OF THE PHYTOPHAGOUS MITES COLLECTED ON CITRUS IN THE WORLD Vincenzo V, Acarologia 50 (2), pp. 221-241 : 225-228

Tenuipalpidae

Twenty four species of Tenuipalpidae have been recorded worldwide from citrus ( Jeppson et al., 1975; Meyer Smith, 1979, 1993; Gahi and Shenhmar, 1984; Gerson, 2003; Mesa et al., 2009; Vacante, 2010) ( Table 2). They are usually considered to be secondary pests, but the ability of some species of the genus Brevipalpus to vector plant viruses has necessitated an updated review of this relatively little known family ( Gerson, 2008). One of these Brevipalpus species is very injurious to citrus in Central and Southern America because it transmits the very pernicious forms of Leprosis (Knorr et al., 1960, 1968; Kitajima et al., 1972; Carter, 1973; Childers et al., 2001, 2003a, 2003b, 2003c). In other regions, like the Mediterranean area ( Vacante, 2009, 2010) or South Africa ( Schwartz, 1977), the economic importance of these species is much less. The reddish black flat mite, B. phoenicis , and the ornamental flat mite, B. obovatus Donnadieu , are major pests, whereas the citrus flat mite, B. californicus (Banks) , is of medium or minor pest status. The grape flat mite, B. chilensis , and the citrus scab mite, B. lewisi , are minor pests. The pest status of the other 19 species is unknown.

Brevipalpus phoenicis is a polyphagous species, with worldwide distribution. The average length of a generation ranges from 27.5 days at 24°C to 18.3 days at 30°C ( Prieto Trueba, 1975). On citrus its injury is similar to that of B. californicus and B. obovatus in Texas ( Dean and Maxwell, 1967; France and Rakhi, 1994; Childers et al., 2003c) and in South Africa ( Schwartz 1970, 1977; Meyer Smith and Schwartz, 1998a). Oranges damaged by reddish black flat mite are usually lighter and their weight is inversely proportional to the degree of infestation, furthermore, affected trees may lose 50% of their yield ( Rodrigues et al., 2003). In Italy Di Martino (1985) has observed greyish scabby patches and cracks on the medial apical epidermis of mandarin fruit. Many lesions are located on oleiferous glands, which are emptied and dried; affected fruits show rounded reddish orange patches.

The greatest risk from a mite attack consists of the transmission of as "Leprosis" or "explosive Lepra" ( Kitajima et al., 1972; Carter, 1973; Boaretto and Chiavegato, 1994; Rodrigues et al.,

as Ma (major), Me (medium), Mi (minor), and U (unknown). For references see Vacante (2010).

1997; Childers et al., 2003c), a viral disease (CiLV- C, CiLV-N) ( Bastianel et al., 2006) recorded in Argentina, Brazil, Paraguay, Venezuela and recently also in Panama. In Florida, the disease has been known since the late 1800’s but there are no records since 1960 ( Morishita, 1954; Childers et al., 2001) and following studies suggest the elimination of the virus from Florida and Texas ( Childers et al., 2003b).

Of the Brevipalpus spp. occurring on citrus only B. phoenicis transmits the virus throughout its different biological stages, but not transovarially, and in order to become infective, each mite has to acquire the virus separately ( Pascon et al., 2006), transmitting it mechanically from citrus plant to citrus plant and/or from a few herbaceous plants of the genera Atriplex , Beta and Chenopodium (Chenopodiaceae) , Gomphrena (Amaranthaceae) , and Tetragon ( Tetragoniaceae ) to citrus ( Childers et al., 2001). Clones of B. phoenicis from Sªo Paolo and from Florida differed in their capacity to transmit CiLV ( Rodrigues et al., 2003), and mite fitness was reduced when it was placed onto new host plants. The phenomenon can be explained by the existence of several hostspecialized clones instead of one generalist form, each adapted to different environments and host plants ( Groot et al., 2005).

In addition, the reddish black flat mite was considered responsible of other disorders, as the " phoenicis blotch" in Florida ( Jeppson et al., 1975), the " Brevipalpus galls" (Knorr et al., 1960, 1968; Knorr and Denmark, 1970) and "halo scab" ( Knorr and Malaguti, 1960; Chiavegato and Kharfan, 1993) in Venezuela; this last disorder is attributed to mite association on fruit of sour orange with scabs of fungus Elsinoe fawcetti Bitanic and Jenkins (Elsinoaceae) . In Honduras B. phoenicis is also associated on sour orange with the same fungus ( Evans et al., 1993), and a similar interaction between mite and fungi has been reported in Costa Rica ( Ochoa et al., 1994) and Brazil ( Chiavegato and Kharfan, 1993).

The damage caused by Leprosis reduces citrus yields in Brazil and more than 60 million dollars are spent each season on chemical sprays applied to control B. phoenicis ( Rodrigues, 2006) . Acaricide applications for the annual control of infestations of this mite represent 35% of total agrochemical costs and 14% of total production costs in mature orchards. Sequential sampling for Leprosis, based on its binomial distribution, deriving from a study of the spatial patterns of Leprosis and of B. phoenicis , indicated that the patterns of the disease and of infested plants deviated from a binomial distribution. Hence, estimates of disease or mite incidence may not be precise ( Bassanezi and Laranjeira, 2007). The need to limit the use of chemicals and their attendant disadvantages have been suggested in Brazil.

In order to promote IPM ( Gravena, 1998), the technical characteristics of the main acaricides registered for citrus and the detailed procedures of a laboratory bioassay conducted to evaluate the efficacy of acaricides against citrus Leprosis mite were suggested (Graven et al., 2005). Other options are to investigate the host plant resistance ( Grewal, 1993; Bastianel et al., 2005, 2006; Rodrigues, 2006).

The main scientific gained experience includes the study of the biology of the pest populations ( Weeks et al., 2000; Groot et al., 2005) and the need of a taxonomic revision of the group based on modern methods of analyzes. For instance, the problem of synonymy in closely related species ( B. phoenicoides Gonzalez , B. phoenicis , B. jordani Dosse , etc.) within the taxonomic revision of the group ( Groot and Breeuwer, 2006).

Brevipalpus obovatus is a polyphagous species with worldwide distribution. At 23 ± 1°C and 60 ± 5% RH, the life cycle from egg to adult takes 27.8 days and at 27°C 21.5 days ( Trindade and Chiavegato, 1994). In Texas the symptoms of its attack on citrus are similar to those of B. phoenicis and B. californicus ( Dean and Maxwell, 1967; France and Rakhi, 1994; Childers, 1994; Childers et al., 2003c). In the USA ( Jeppson et al., 1975), South Africa (Meyer Smith and Schwartz, 1998b) and Mediterranean region the ornamental flat mite does not cause serious damage to citrus. Although in Argentina the injury of B. obovatus feeding on citrus leaves, fruits and twigs has been defined as "Lepra explosive" or "Leprosis" ( Vergani, 1945) it is improperly considered responsible for the transmission of citrus Leprosis, as its ability to transmit the virus was not proven ( Childers et al., 2001). In Venezuela the ornamental flat mite is associated with "halo scab", but when B. obovatus and B. phoenicis are present on the same plant, the damage to the leaves and stems is more severe and primarily due to the latter species (Knorr et al., 1960).

Brevipalpus californicus has a worldwide distribution and similarly to other treated Tenuipalpids is a polyphagous species. At 23 ± 1°C and 60 ± 5% RH, the life cycle from egg to adult develops in 26.5 days and at 27°C in 21 days ( Trindade and Chiavegato, 1994). In Australia ( Jeppson et al., 1975), South Africa ( Schwartz, 1977) and in the Mediterranean region ( Di Martino, 1985) it causes brown to bronze colored and corky scab-like spots on rind of sweet orange. Feeding by mite produces a silvering of the fruit, particularly of lemon. In Texas the citrus flat mite has been associated with rind spotting of oranges and grapefruit, first yellowish and discoloured in depression on the fruit surface and tending to become darker in color.

In the American Continent the mite is feared for risk of transmitting the Leprosis virus to citrus leaves and fruit, which has strongly limited the development of citrus groves in certain areas of the world ( Knorr et al., 1968). In Texas and Florida on grapefruit and orange varieties it produces smaller necrotic lesions form on the surface of infested leaves and fruits, called "Leprosis-like spotting" or "nail head rust" ( Dean and Maxwell, 1967; Jeppson, 1989; France and Rakhi, 1994). In Florida, the symptoms on twigs and branches are is indicated as Ma (major), Mi (minor), and U (unknown). For references see Vacante (2010).

called "Florida scaly bark" and in Argentina both symptoms are known as "Lepra explosive" or "Leprosis".

However, the pest does not transmit viral diseases and at present the only known vector of the disease is B. phoenicis ( Rodrigues et al., 2003).

Brevipalpus chilensis has been recorded in the Oriental and Neotropical regions, where it is responsible for the silvering of citrus fruits. It is a polyphagous species and depending on the climatic conditions completes its life cycle in a range of 18-59 days (Gonzalez, 1968). The mite does not transmit diseases.

Brevipalpus lewisi is a polyphagous species, with worldwide distribution. Its optimal net reproductive rate (R 0) is 4.82 and occurs at 22°C and 70% RH ( Buchanan et al., 1980). High densities of the citrus scab mite cause large alterations on the surface of the citrus fruit, reducing seriously the quality of fruit. The pest does not cause damage to leaves or wood and the scablike scars observed on most varieties of citrus rarely occur on grapefruit ( Elmer and Jeppson, 1957). On tangerines the citrus scab mite causes grade-reducing scarring on 17-28% of the fruit (16-21% of navel oranges, 18-35% of grapefruits) ( Elmer, 1968); on Lisbon lemon fruits, scarring may affect over 25% of the fruit ( Lewis, 1949). The pest does not transmit diseases.

The natural enemies of the Tenuipalpids include fungi (Ascomycota, Clavicipitaceae ), insects ( Coccinellidae ) and mites ( Cheyletidae , Phytoseiidae , Stigmaeidae , Tydeidae ) ( Vacante, 2010). In Egypt the Phytoseiid Euseius scutalis (Athias Henriot) controlled B. californicus after 50 predator individuals were released per citrus tree ( El-Halawany et al., 1993). However, most growers lack practical experience in biological control and the control of Tenuipalpid populations is done normally by chemical means; this is also considered safer in order to reduce the risk of disease transmission.