Invasive Species Compendium

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Datasheet

Citrus leprosis virus C
(leprosis of citrus)

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Datasheet

Citrus leprosis virus C (leprosis of citrus)

Summary

  • Last modified
  • 27 September 2018
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Citrus leprosis virus C
  • Preferred Common Name
  • leprosis of citrus
  • Taxonomic Tree
  • Domain: Virus
  •   Family: Unassigned virus family
  •     Genus: Cilevirus
  •       Species: Citrus leprosis virus C
  • Summary of Invasiveness
  • CiLV-C is a quarantine pest which causes an economically important disease, reported only on the American continent. During the past 15 years, it has caused economic losses in Brazil, Argentina, Paraguay, Uruguay, Ven...

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Pictures

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PictureTitleCaptionCopyright
Citrus leprosis virus C; symptoms in a sweet orange fruit. Sao Paulo State, Brazil.
TitleSymptoms
CaptionCitrus leprosis virus C; symptoms in a sweet orange fruit. Sao Paulo State, Brazil.
Copyright©José Carlos Verle Rodrigues
Citrus leprosis virus C; symptoms in a sweet orange fruit. Sao Paulo State, Brazil.
SymptomsCitrus leprosis virus C; symptoms in a sweet orange fruit. Sao Paulo State, Brazil.©José Carlos Verle Rodrigues
Citrus leprosis virus C; symptoms in a sweet orange leaf. Sao Paulo State, Brazil.azil.
TitleSymptoms
CaptionCitrus leprosis virus C; symptoms in a sweet orange leaf. Sao Paulo State, Brazil.azil.
Copyright©José Carlos Verle Rodrigues
Citrus leprosis virus C; symptoms in a sweet orange leaf. Sao Paulo State, Brazil.azil.
SymptomsCitrus leprosis virus C; symptoms in a sweet orange leaf. Sao Paulo State, Brazil.azil.©José Carlos Verle Rodrigues
Citrus leprosis virus C; symptoms in a sweet orange branch. Sao Paulo State, Brazil.
TitleSymptoms
CaptionCitrus leprosis virus C; symptoms in a sweet orange branch. Sao Paulo State, Brazil.
Copyright©José Carlos Verle Rodrigues
Citrus leprosis virus C; symptoms in a sweet orange branch. Sao Paulo State, Brazil.
SymptomsCitrus leprosis virus C; symptoms in a sweet orange branch. Sao Paulo State, Brazil.©José Carlos Verle Rodrigues
Citrus leprosis virus C; transmission electron micrograph of  virus like particles (VLP) associated with symptoms of Citrus leprosis in leaf of sweet orange; (CW = cell wall.)
TitleVirus-like particles associated with Citrus leprosis
CaptionCitrus leprosis virus C; transmission electron micrograph of virus like particles (VLP) associated with symptoms of Citrus leprosis in leaf of sweet orange; (CW = cell wall.)
Copyright©José Carlos Verle Rodrigues
Citrus leprosis virus C; transmission electron micrograph of  virus like particles (VLP) associated with symptoms of Citrus leprosis in leaf of sweet orange; (CW = cell wall.)
Virus-like particles associated with Citrus leprosisCitrus leprosis virus C; transmission electron micrograph of virus like particles (VLP) associated with symptoms of Citrus leprosis in leaf of sweet orange; (CW = cell wall.)©José Carlos Verle Rodrigues
Citrus leprosis virus C; scanning electron micrograph of vector, the mite Brevipalpus phoenicis.
TitleVector
CaptionCitrus leprosis virus C; scanning electron micrograph of vector, the mite Brevipalpus phoenicis.
Copyright©José Carlos Verle Rodrigues
Citrus leprosis virus C; scanning electron micrograph of vector, the mite Brevipalpus phoenicis.
VectorCitrus leprosis virus C; scanning electron micrograph of vector, the mite Brevipalpus phoenicis. ©José Carlos Verle Rodrigues

Identity

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Preferred Scientific Name

  • Citrus leprosis virus C

Preferred Common Name

  • leprosis of citrus

Other Scientific Names

  • Citrus leprosis virus cytoplasmic
  • Citrus leprosis virus cytoplasmic type 2
  • Citrus leprosis virus nuclear

International Common Names

  • Spanish: leprosis, lepra de los citricos
  • French: léprose des agrumes
  • Portuguese: leprose dos citros

Local Common Names

  • Argentina: lepra explosiva de los citricos
  • Panama: leprosis de los citricos

English acronym

  • CiLV-C
  • CiLV-C2
  • CiLV-N

EPPO code

  • CILV00 (Citrus leprosis ?rhabdovirus)

Summary of Invasiveness

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CiLV-C is a quarantine pest which causes an economically important disease, reported only on the American continent. During the past 15 years, it has caused economic losses in Brazil, Argentina, Paraguay, Uruguay, Venezuela, Costa Rica, Panamá and Honduras. The disease was recently reported in Guatemala, Bolivia, México, Colombia and Belize. It is a threat to citrus-producing countries where the disease has not been reported. The disease can cause 100% yield loss (Rodrigues, 2000).

CiLV does not appear to move systemically in the host plant but can move short distances from a grafted shoot tip to the adjacent scion tissue. Accordingly, movement in latently infected planting material is not likely to be a major pathway for CiLV. Citrus leprosis, because of its non-systemic infection, can only be important where attacks by its vector mites are significant. The main means of movement and dispersal of the virus is via the vector mites of the genus Brevipalpus, which colonize most species of Citrus and many other plant species.

Taxonomic Tree

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  • Domain: Virus
  •     Family: Unassigned virus family
  •         Genus: Cilevirus
  •             Species: Citrus leprosis virus C

Notes on Taxonomy and Nomenclature

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Current research shows Citrus leprosis disease symptoms can be caused by two separate viruses, a more common cytoplasmic virus termed Citrus leprosis virus C (CiLV-C) and a rarer, nuclear virus termed Citrus leprosis virus N (CiLV-N) (Pascon et al., 2006). Roy et al. (2013) recently found and described the genome sequence and structure of a new bipartite RNA Citrus leprosis virus; phylogenetic analysis indicated that the new virus was related to CiLV-C. They suggested that the virus be called Citrus leprosis virus Cytoplasmic Type 2 (CiLV-C2) which is a member of the Cilevirus genus.

According to its morphology, CiLV-C has been considered part of the family Rhabdoviridae. However, Locali et al. (2005) suggest that the virus has an RNA with a bipartite genome, unlike the typical monopartite Rhabdovirus genome. This was recently confirmed by complete CiLV-C genome sequence and phylogenetic analysis (Bastianel et al., 2006; Pascon et al., 2006). The complete CiLV-C nucleotide sequence confirms that the virus has a bipartite RNA; RNA 1 contains two open reading frames (ORFs) corresponding to 286 and 29 kDa, and RNA 2 contains four ORFs corresponding to 15, 61, 32 and 24 kDa. Phylogenetic analysis suggests that Citrus leprosis virus is a member of a distinct, novel virus genus and family, does not belong to the Rhabdoviridae family as previously proposed, and should be considered a type of a new genus of viruses, the Cilevirus (Locali et al., 2006). According to Bastianel et al. (2010), this classification has been approved by the executive committee of the ICTV (2008) and is awaiting ratification.

Description

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Presumed virus particles mostly occur in parenchyma cells of the lesion in affected orange leaves, fruits or stems. Particles are short, bacilliform, 120-130 nm long (occasionally up to 300 nm) and 50-55 nm wide. They occur within the lumen of the endoplasmic reticulum (Kitajima et al., 1974; Colariccio et al., 1995). There is a report of similar but unenveloped particles in the nucleoplasm (Kitajima et al., 1972).

In addition to the presence of the rhabdovirus-like particles within the endoplasmic reticulum of tissues from the lesion, dense viroplasm-like material is commonly found in the cytoplasm, near the particles. Small vesicle-containing fibrillar materials are frequently present in the vacuole, associated with the tonoplast, next to the dense material (Kitajima et al., 1972; Colariccio et al., 1995).

Chloroplasts are usually affected with a disorganized hypertrophied lamella system (Kitajima et al., 1972; Rodrigues, 1995). There is a report in which rod-like particles, considered to be naked rhabdovirus particles accumulate in the nucleoplasm associated with the nuclear envelope (Kitajima et al., 1972).

Kitajima et al. (1972) were the first to describe leprosis virions in citrus leaves as particles resembling those of rhabdoviruses, but shorter, occurring in the nucleus or cytoplasm, and associated with the presence of a viroplasm in the nucleus of the cells. After this initial report, Kitajima (1974) and Colariccio et al. (1995) revealed the presence of short, bacilliform particles in the endoplasmic reticulum and dense viroplasm in the cytoplasm, rather than in the nucleus, of infected cells. This virus, known as the cytoplasmic  type (CiLV-C), has been shown to be prevalent in citrus orchards, whereas the nuclear type (CiLV-N) described in 1972, is of rare occurrence (Rodrigues et al., 2003).

Distribution

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Citrus leprosis virus (CiLV-C) is a quarantine pest and economically important disease, reported only on the American continent. During the past 15 years, it has caused economic losses in Brazil, Argentina, Paraguay, Uruguay, Venezuela, Costa Rica, Panamá and Honduras. The disease was recently reported in Guatemala, Bolivia, México, Colombia and Belize.

CABI has been informed by the Servicio Nacional de Sanidad Agraria (SENASA) that the record for Peru in CABI/EPPO (2000) and EPPO (2003) is incorrect. This record was based on Bové and Vogel (1980) and, in the absence of details of the virus isolation and corroborating reports for Peru, the record has been omitted from the map.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/RegionDistributionLast ReportedOriginFirst ReportedInvasiveReferenceNotes

North America

MexicoRestricted distribution2005Izquierdo et al., 2011; CABI/EPPO, 2013; EPPO, 2014CiLV-C in Tabasco.
USAAbsent, formerly presentCABI/EPPO, 2013; EPPO, 2014
-FloridaAbsent, formerly presentFawcett, 1911; Knorr, 1968; CABI/EPPO, 2013; EPPO, 2014
-MississippiAbsent, formerly presentEPPO, 2009; Bitancourt, 1955; EPPO, 2014

Central America and Caribbean

BelizeRestricted distributionEPPO, 2012; CABI/EPPO, 2013; EPPO, 2014
Costa RicaPresentAraya Gonzáles, 2000; CABI/EPPO, 2013; EPPO, 2014
El SalvadorPresentCABI/EPPO, 2013; EPPO, 2014
GuatemalaPresentMejia et al., 2005; CABI/EPPO, 2013; EPPO, 2014
HondurasRestricted distributionCABI/EPPO, 2013; EPPO, 2014
NicaraguaPresentIPPC, 2007; CABI/EPPO, 2013; EPPO, 2014
PanamaPresentDominguez et al., 2000; Dominguez et al., 2001; CABI/EPPO, 2013; EPPO, 2014

South America

ArgentinaPresentCáceres, 1998; Vergani, 1945; Bitancourt, 1955; CABI/EPPO, 2013; EPPO, 2014
BoliviaRestricted distribution2005Bitancourt, 1955; Gómez et al., 2005; CABI/EPPO, 2013; EPPO, 2014
BrazilWidespreadCABI/EPPO, 2013; EPPO, 2014
-AcrePresentCABI/EPPO, 2013; EPPO, 2014
-AmazonasPresentCABI/EPPO, 2013; EPPO, 2014
-BahiaPresentCABI/EPPO, 2013; EPPO, 2014
-CearaPresentCABI/EPPO, 2013; EPPO, 2014
-Espirito SantoPresentCABI/EPPO, 2013; EPPO, 2014
-GoiasPresentCABI/EPPO, 2013; EPPO, 2014
-Mato GrossoPresentCABI/EPPO, 2013; EPPO, 2014
-Mato Grosso do SulPresentCABI/EPPO, 2013; EPPO, 2014
-Minas GeraisPresentBitancourt, 1940; CABI/EPPO, 2013; EPPO, 2014
-ParaPresentBitancourt, 1940; CABI/EPPO, 2013; EPPO, 2014
-ParanaPresentIAPAR, 1992; CABI/EPPO, 2013; EPPO, 2014
-PiauiPresentBitancourt, 1955; CABI/EPPO, 2013; EPPO, 2014
-Rio de JaneiroPresentBitancourt, 1955; CABI/EPPO, 2013; EPPO, 2014
-Rio Grande do SulPresentFawcett & Bitancourt, 1937; Moraes, 1998; CABI/EPPO, 2013; EPPO, 2014
-RondoniaPresentTeixeira et al., 1993; CABI/EPPO, 2013; EPPO, 2014
-RoraimaPresentCABI/EPPO, 2013; EPPO, 2014
-Santa CatarinaPresentCABI/EPPO, 2013; EPPO, 2014
-Sao PauloWidespreadRodriques, 2000; Bitancourt et al., 1933; CABI/EPPO, 2013; EPPO, 2014
-SergipePresentCABI/EPPO, 2013; EPPO, 2014
-TocantinsPresentDomingues & Rodriques, 1999; CABI/EPPO, 2013; EPPO, 2014
ColombiaRestricted distributionLeón et al., 2006a; Leon et al., 2006b; CABI/EPPO, 2013; EPPO, 2014
ParaguayPresentSpegazzini, 1920; CABI/EPPO, 2013; EPPO, 2014
PeruAbsent, invalid recordCABI/EPPO, 2013; EPPO, 2014
UruguayPresentBitancourt, 1940; CABI/EPPO, 2013; EPPO, 2014
VenezuelaPresentBitancourt, 1955; CABI/EPPO, 2013; EPPO, 2014

Europe

NetherlandsAbsent, confirmed by surveyEPPO, 2014

Risk of Introduction

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CiLV-C is an economically important disease, which represents millions of dollars in damage to citrus crops in countries where it has been established, affecting mainly oranges and mandarins. Is a threat to citrus producing countries where the disease has not been reported. Several authors (Rodrigues et al., 2001; Freitas et al., 2004) consider CiLV-C as the most important viral disease in the Brazilian citrus industry because the costs of controlling the mite vector reach about US $90 million dollars per year.

CiLV has not been considered to be a quarantine pest by any regional plant protection organization, but it is under evaluation for the EPPO A1 list. Doubts about the aetiology of leprosis have probably contributed to this situation. Feeding by the vector mites alone does cause certain symptoms, and this has probably complicated the recognition that, in some countries, a virus is also present and causes distinct symptoms.

The vector mites are present in some EPPO countries but appear to be of no practical importance as pests of citrus. They are pests which are apparently more favoured by a warm, humid climate. To a certain extent, control of more important mites (for example, Panonychus citri) may also be eliminating them. However, it is clear that citrus leprosis, because of its non-systemic infection, can only be important where attacks by its vector mites are significant. For this reason, the risk to citriculture in the EPPO region from CiLV appears low.

Flat mites, Brevipalpus spp., are dispersed worldwide. Three species Brevipalpus californicus, B. obovatus and B. phoenicis have been reported as vectors of citrus leprosis, but only B. phoenicis has proven to be an efficient vector. Several Brevipalpus type species within B. phoenicis have been identified worldwide distribution in recent years (Beard et al., 2012). This means the need for more intensive research to identify the extent of this species complex. More guidelines are needed for the inspection and movement of live plant materials that are host plants for Brevipalpus mites from one country to another (Childers and Rodrigues, 2011).

Phytosanitary Measures

If it is considered useful to take measures against CiLV, then it should be sufficient to require that any imported plants for planting of citrus should be free from leprosis lesions and originate from nurseries found free from, and/or treated against, Brevipalpus mites during the growing season. The risk from normal commercial consignments of fruits seems insignificant. In practice, citrus from countries where CiLV occurs is already subject to strict requirements on account of more serious pests.

Habitat List

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CategoryHabitatPresenceStatus
Terrestrial-managed
Cultivated / agricultural land Principal habitat Harmful (pest or invasive)

Hosts/Species Affected

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Citrus species, especially sweet oranges (Citrus sinensis) are naturally infected by CiLV. Lemons (C. limon), mandarins (C. reticulata, C. reshni, C.deliciosa), grapefruits (C. paradisi) and hybrids (for example, Murcott) are much less susceptible under natural conditions (Rodrigues et al., 1998). No other plant species is known to serve as a natural host for the agent causing citrus leprosis. Recently, local lesions have been induced with some difficulty from several herbaceous hosts (Chenopodium amaranticolor, C. quinoa, Gomphrena globosa) when mechanically inoculated (Colariccio et al., 1995).

 A few years ago, it was thought that CiLV-C only affected citrus Rutaceae plants. Colariccio et al. (1995) were able to mechanically transmit the virus from sweet orange to sweet orange and to herbaceous host and indicator plants such as Chenopodium amaranticolor [C. giganteum], C. quinoa and Gomphrena globosa. Lovisolo et al. (2000) expanded the number of known hosts of the virus to 13 species of 5 different genera including G. globosa (Amaranthaceae), Tetragonia tetragonoides (Tetragoniaceae), Atriplex hortensis, A. latifolia, Beta vulgaris ssp. cycla and Chenopodium bonus-henricus (Chenopodiaceae), as new experimental host records for CiLV. They achieved mechanical inoculation in these species, but failed in transmission of the virus back to citrus plants. The same authors further assert that mechanical transmission of the virus from citrus plants is possible but at a very low percentage.

Maia and Oliveira (2006) evaluated the potential of some common plants (hedgerows, windreaks and weeds) in and around citrus orchards as hosts of CiLV, and transmission of the disease to orange by Brevipalpus phoenicis. The following plants were included in the trials: Hibiscus sp., Malvaviscus mollis [M. arboreus], Grevillea robustaMimosa caesalpiniifoliaBixa orellanaCommelina benghalensisBidens pilosaSida cordifolia and Ageratum conyzoides. Mites were reared on infected citrus fruits, and transferred to leaves from the tested host plants. Mites were subsequently transferred to orange cultivars Natal and Valencia and these plants were raised in the greenhouse. Mites reared on non-infected fruits were allowed to feed on the host plant leaves during 3 days and then transferred to orange seedlings. After 60 days, lesions on oranges were counted. Mites continued to transfer the virus to orange seedlings even at 7 days after feeding on the host plants. Mites reared on non-infected fruits acquired the virus and transmitted this to orange plants when the host plants used were C. benghalensisA. conyzoidesB. pilosa, S. cordifolia or B. orellana leaves, on which pests reared on infected fruits were previously grown.

The first non-citrus natural host of CiLV was reported in Colombia, in plants of Swinglea glutinosa. This plant is used in hedgerows throughout Colombia, also near citrus orchards, thus the report is a concern to the spread of citrus leprosis in the coutry (León et al., 2008).

Freitas et al. (2009) reported the citroid fruit tree Glycosmis pentaphylla as a host of CiLV-C and stated that the plant exhibits novel leprosis symptoms. Nunes et al. (2012a) found susceptibility to CiLV in several non-citrus plants. Leprosis symptoms on leaves of Hibiscus rosa-sinensis, M. arboreus, G. robusta and B. orellana, appeared when these hosts were infested by viruliferous B. phoenicis mites. RT-PCR and electron microscope analyses confirmed the presence of CiLV-C in these plants.

Nunes et al. (2012b) report the presence of leprosis symptoms in a perennial weed native of tropical Asia and Africa, tropical spiderwort (C. benghalensis), commonly found in citrus groves in Brazil. The presence of CiLV-C was naturally and experimentally confirmed with RT-PCR detection techniques. This report explains that other plants or weeds grow within or near citrus orchards may be susceptible to CiLV and may serve as a host of B. phoenicis, so these plants may play an important role in the spread of the disease.

Host Plants and Other Plants Affected

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Growth Stages

Top of page Fruiting stage, Vegetative growing stage

Symptoms

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Round to elliptical local lesions are seen on fruits, leaves and twigs. The severity of the lesions varies with the type of citrus and the region of origin. Leaf symptoms are usually round with a dark-brown central spot about 2-3 mm diameter, surrounded by a chlorotic halo, in which 1-3 brownish rings frequently appear surrounding the central spot; the overall lesion size varies from 10 to 30 mm, though larger lesions may form by the fusion of 2 or more adjacent lesions.

On fruits, lesions are necrotic spots 10-20 mm in diameter, with a necrotic centre. Gum exudation is occasionally observed on the lesion. On green fruits, the lesions are initially yellowish, becoming more brown or black, sometimes depressed, and reducing the market value of the fruits.

On stems, lesions may be protuberant, cortical, grey or brown. Lesions may coalesce when present in large numbers, leading to the death of the twig. In extreme cases observed in different places (JCV Rodrigues, personal communication), as described initially in 'lepra explosiva' in Argentina, severe defoliation and fruit fall may occur (Frezzi, 1940; Bitancourt, 1955; Rossetti et al., 1969).

Citrus leprosis lesions are usually very characteristic, but may sometimes be mistaken for lesions of citrus canker caused by the bacterium Xanthomonas axonopodis pv. axonopodis, or zonate chlorosis (Rossetti, 1980). Zonate chlorosis, which is associated with infestation by the same mites, does not become necrotic. Symptoms are essentially concentric green and chlorotic rings (Bitancourt, 1934).

Other viral diseases are vectored by Brevipalpus phoenicis in Brazil. Coffee ringspot virus in Coffea arabica (Chagas, 1978); Ligustrum ringspot virus in Ligustrum lucidum (Rodrigues et al., 1995); and green spot of passion fruit in Passiflora edulis (Kitajima et al., 1997). In addition, Brevipalpus californicus is a vector of Orchid fleck virus in orchids (Maeda et al., 1998). However, cross-transmission was not described among these viruses and leprosis.

List of Symptoms/Signs

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SignLife StagesType
Fruit / lesions: scab or pitting
Fruit / premature drop
Growing point / dieback
Leaves / abnormal patterns
Leaves / necrotic areas
Stems / canker on woody stem
Stems / gummosis or resinosis
Whole plant / plant dead; dieback

Biology and Ecology

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Citrus leprosis is always associated with infestation by a false spider mite of the genus Brevipalpus. Knorr (1950) reported that Brevipalpus is associated with citrus leprosis in Florida, USA. He also later demonstrated that Brevipalpus obovatus collected from Bidens pilosa was able to induce citrus leprosis symptoms and that B. californicus was the reported vector of leprosis in Florida, USA (Knorr, 1968). However, those symptoms, unusually, were only observed a long time after mite infestation. This led to speculation about possible mite contamination during the transmission tests.

The same mite species was found associated with citrus leprosis in Argentina (Knorr and Ducharme, 1951). In Brazil, Musumeci and Rossetti (1963) showed that B. phoenicis transmitted the disease under experimental conditions and that natural infestation of orchards by this mite was associated with the incidence of citrus leprosis. The larvae were reported as more efficient vectors than adults and nymphs by Chagas et al. (1984) but Chiavegato (1995) concluded that this was not true.

The mites are parthenogenetic (females producing females) with males rarely found (Pijnaker et al. 1981). B. lewisi occurs in California citrus and has never been incriminated with vectoring leprosis. B. chilensis has been reported on citrus in Chile (Jeppson et al. 1975).

Reproduction of Brevipalpus mites is by thelytoky parthenogenesis, i.e., female lay eggs that will lead to genetically similar females (Helle et al., 1980). Apparently, the females are haploid and they only have two chromosomes (Pijnacker et al., 1980, 1981). Populations of mites from different hosts present a high degree of polymorphism in fragments of DNA amplified by PCR and they possess different capacities of colonization on different host plant species (Rodrigues et al., 1996).

The disease is characterized by lesions in leaves, twigs and fruits which do not become systemic. Its aetiology has been controversial, since the cause has been considered to be either a toxin produced by the mite, or localised infection with a virus transmitted by the mite. Several pieces of experimental evidence support viral aetiology: only mites which have access to lesions cause leprosis (Rossetti et al., 1959); tip grafting of infected shoots results in spread from the graft to the receptor tissue (Knorr, 1968; Chagas and Rossetti, 1980); lesions can be experimentally reproduced by mechanical transmission from citrus to citrus and from citrus to several herbaceous plants (Colariccio et al., 1995); and unenveloped or enveloped rhabdovirus-like particles have been consistently found in cells from citrus leprosis lesions of citrus fruit, leaf or stem (Kitajima et al., 1972, 1974; Colariccio et al., 1995). The same type of particle was found in both inoculum tissue and in the lesions produced by mechanical transmission (Colariccio et al., 1995). Indirect evidence is that the mite vectors occur in many parts of the world where leprosis has never been recorded.

Large numbers of particles similar to CiLV occur within the bodies of viruliferous mites (Rodrigues et al., 1997). When originating from eggs, Brevipalpus mites do not have particles present within their bodies nor do they transmit virus. This indicates that the virus is not transovarially transmitted (Rodrigues, 2000). Mites that acquire the virus have the ability to transmit for their lifetime, even if only feeding on non-virus hosts plants and after successive moults (Rodrigues, 1995). All this information, suggests that the virus is of the circulative type, not only accumulating, but also multiplying inside the body of the mite vector.

Climate

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ClimateStatusDescriptionRemark
A - Tropical/Megathermal climate Preferred Average temp. of coolest month > 18°C, > 1500mm precipitation annually
Cf - Warm temperate climate, wet all year Tolerated Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year
Cs - Warm temperate climate with dry summer Tolerated Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter Preferred Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)

Means of Movement and Dispersal

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CiLV apparently only infects plants locally, each lesion being associated with infestation by a vector mite. The virus does not appear to move systemically in the host plant but can move short distances from a grafted shoot tip to the adjacent scion tissue. Accordingly, movement in latently infected planting material (as very commonly occurs for most plant viruses) is not likely to be a major pathway for CiLV.

In practice, the main means of movement and dispersal is via the vector mites of the genus Brevipalpus. These colonize most species of Citrus and many other plant species. According to Oliveira (1986), Brevipalpus mites have been found infesting more than 200 different plant species. Chiavegato and Kharfan (1993) reported that fruits with scab lesions (Elsinoë fawcettii) were preferred for colonization by mites.

According to Childers et al. (2003), the flat mites Brevipalpus californicus, B. obovatus and B. phoenicis have 928 plant species recorded as hosts worldwide. The most important CiLV-C vector mite, B. phoenicis is able to live and multiply in 486 host plants besides citrus. Among cultivated plants, they mention cashew, mango, papaya, cassava, cotton, guava, passion fruit, coffee, cacao and grape. In Brazilian citrus orchards, there are important weeds such as sabia (Mimosa caesalpiniaefolia), mallow (Malvaviscus arboreus), bala (Sida cordifolia), dayflower (Commelina benghalensis), goatweed (Ageratum conyzoides) and marigold spanish needle (Bidens pilosa) which are common hosts of the red flat mite (Maia and Oliveira, 2002). Ulian and Oliveira (2002) found that B. phoenicis lives in citrus windbreaks and so recommended that Hibiscus sp. and Bixa orellana should not be used as living barriers because they favour survival of the mite. León et al. (2006a) recorded several weed hosts of the mite in citrus orchards such as verbena (Stachytarpheta cayennensis) yerbamora (Lantana camara) and escobo (Sida spp.). Natural infection of CiLV-C and the presence of the mite in Swinglea glutinosa plants, which are used in Colombia as a living fence, have also been reported (León et al., 2008).

The epidemic development of the disease, analysed by Rodrigues (2000) in orchards without chemical control of the vector, was better adjusted for the logistic model (Vanderplank, 1963), whose biological interpretation indicated that the speed of increase of the disease is proportional to the level of disease and the amount of available healthy tissues.

In international trade, CiLV is unlikely to be latently carried on citrus budwood. Normal nursery management procedures should ensure that budwood material showing symptoms does not enter trade. CiLV is possibly more likely to be spread on rooted plants since these are more likely to carry vector mites and may be harder to inspect for symptoms. Infected plants would be most likely to come from nurseries which have not been treated against mites. Since little is known about alternative hosts for the virus, some of which may be asymptomatic carriers, there may be some risk of introducing citrus leprosis via other plant species. However, this is considered to be unlikely. Other plant species could possibly also carry viruliferous mites, since the mites concerned are polyphagous and could move from citrus to other hosts. CiLV is not transmitted in seeds.

Citrus fruits are selected and processed in packing houses before export and this eliminates the mites. Thus, it is unlikely that CiLV would be introduced with green fruits, branches or leaves, because the mites are unable to acquire the virus from mature fruits.

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Crop productionInfected mites can be carried in seedlings from citrus nurseries to farmers' fields. Yes
Hedges and windbreaks Yes
HitchhikerThe infected mite vector can be transported in many ways (fruit, vegetables, host plants, clothes, e Yes Yes
Ornamental purposesInfected mite vector can be transported in ornamental host plants. Yes Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
Aircraft Yes Yes
Clothing, footwear and possessionsInfected mite vector is frequently transported in clothes. Yes
Containers and packaging - non-wood Yes
Plants or parts of plantsViruliferous vectors. Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Flowers/Inflorescences/Cones/Calyx Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Fruits (inc. pods) Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Leaves Yes Pest or symptoms usually invisible
Stems (above ground)/Shoots/Trunks/Branches Yes Pest or symptoms not visible to the naked eye but usually visible under light microscope
Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
Growing medium accompanying plants
Roots
Seedlings/Micropropagated plants
True seeds (inc. grain)
Wood

Vectors and Intermediate Hosts

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VectorSourceReferenceGroupDistribution
Brevipalpus phoenicisMite

Impact Summary

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CategoryImpact
Economic/livelihood Negative

Impact

Top of page If proper mite control is not undertaken when the disease first appears, severe losses in quantity and quality of yield may occur. Fruits with lesions have low commercial value, especially for direct consumption. In severe cases, twigs may die, jeopardising future fruit production. Furthermore, untreated orchards may serve as a source for the mite and citrus leprosis may spread to other plantations in the area.

Citrus leprosis usually occurs in cycles; when citrus prices are high, growers control the mites but when prices fall, chemical treatments for mites and other pests and pathogens are applied to a lesser extent and the incidence of citrus leprosis increases. In São Paulo State, Brazil, when there is inoculum in the area and miticides are not sprayed, 2-3 years are enough to completely spread the disease in the orchard. The large orchards contribute to the occurrence and spread of the disease in the São Paulo citrus industry.

The disease is reported to be particularly important in Brazil and Argentina. It has no current importance in the USA, where there have been no recent reports. More than 60% of the orchards in the State of São Paulo have leprosis symptoms (Salva and Massari 1995). Because of its widespread occurrence, potential high damage, according to the susceptibility of the citrus variety, isolate and inefficient chemical control of the vector, the disease can cause 100% yield losses (Rodrigues, 2000).

Risk and Impact Factors

Top of page Invasiveness
  • Proved invasive outside its native range
  • Has a broad native range
  • Abundant in its native range
  • Highly adaptable to different environments
  • Is a habitat generalist
  • Tolerant of shade
  • Capable of securing and ingesting a wide range of food
  • Highly mobile locally
  • Long lived
  • Fast growing
  • Has high reproductive potential
  • Has high genetic variability
Impact outcomes
  • Host damage
  • Increases vulnerability to invasions
  • Negatively impacts agriculture
  • Negatively impacts cultural/traditional practices
  • Damages animal/plant products
  • Negatively impacts trade/international relations
Impact mechanisms
  • Pest and disease transmission
  • Pathogenic
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Highly likely to be transported internationally deliberately
  • Difficult to identify/detect as a commodity contaminant
  • Difficult to identify/detect in the field
  • Difficult/costly to control

Detection and Inspection

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Citrus leprosis is principally detected by the observation of characteristic local lesions. It can be mechanically transmitted in extracts from infected tissue frozen in liquid nitrogen, with tris or phosphate buffer containing several reducing agents, to induce lesions on orange and some herbaceous hosts (Chenopodium amaranticolor [C. giganteum], C. quinoa and Gomphrena globosa).

Electron microscopy of lesion tissues reveals virus-like particles in parenchyma cells (Colariccio et al., 1995) or in the nucleoplasm, indicating two different particles associated with citrus leprosis (Dominguez et al., 2000).

However, these methods have more significance in relation to research on the aetiology of leprosis than as practical means of detection. No serological tests are available. Seedlings of citrus varieties such as Cleopatra mandarin and Seleta or Pêra sweet oranges were used as susceptible woody indicators when infested by viruliferous mite populations (Rodrigues, 2000).

The viruses transmitted by Brevipalpus induce local symptoms in host plants, being generally restricted to the surrounding areas of the lesions. However, often symptoms do not appear, and the virus remains latent. These reactions of the plant seem to be associated with the plant genotype and the age of the tissue on the infection time. Because of the low titre in the host plants, it has not been possible to efficiently isolate or characterize the virus.

Starting from the isolation of dsRNA molecules associated with CiLV infection in citrus seedlings (Rodrigues et al., 2000), tools for the characterization of the virus have been developed and the relationships between the plant and the vector understood. Two different kinds of virus particles were found associated with leprosis symptoms, one nuclear type (Kitajima et al. 1972) and another cytoplasmatic type (Colariccio et al., 1995). Until recently only the cytoplasmic type was experimentally transmitted by Brevipalpus mites (Rodrigues, 2000).

Reverse-transcriptase polymerase chain reaction (RT-PCR)-based diagnosis methods have been developed (Antonioli-Luizon et al., 2004; León et al., 2006). Locali et al. (2003) concluded that RT-PCR was specific, accurate, rapid and reliable for the detection of CiLV. However, Antonioli-Luizon et al. (2004) noted that a limiting factor for RT-PCR methods is the requirement of high quality samples.

Prevention and Control

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Citrus leprosis is basically controlled by controlling the mite vectors. Sprays are applied after field monitoring of the vector once it reaches economic threshold levels. Some IPM programmes include mite predator monitoring in regular field inspections.

Most of the currently available chemicals used to control mites are effective. Some of the products recommended in Brazil are acrinatrin, azocyclotin, bifentrin, cyhexatin, dicofol, hexythiazox, fenbutatin oxide, propargite and quinomethionate (Prates and Rodrigues, 1996). Additional practices are useful to reduce virus inoculum: to remove, by pruning, affected branches; windbreaks to reduce vector spread; control of weeds (alternative mite hosts); use of healthy plants to plant the orchards; and control of the movement of people and material in orchards.

Analyses of mite infestation from non sprayed plants in experimental fields revealed significant differences among sweet orange varieties. In the same manner, disease severity showed high degrees of variability among nine commercial sweet orange varieties (Rodrigues, 2000).

The management strategy of pest agrochemical resistance is essential in managing the leprosis mite. There are several reports of pest resistance to organoestanic acaricides (cyhexatin, fenbutatin oxide, azocyclotin) in Brazil. Mite resistance has already been detected and characterized to dicofol, propargite and hexythiazos acaricides (Omoto et al., 2000). In addition, reduced mite susceptibility was found to enxofre pyrethroid acaricides, lime sulfur, as well as abamectin. In Brazil, the intense use of abamectin and enxofre for citrus rust mite control has already ended in critical points of resistance levels (Omoto and Alves, 2004).

Biological alternatives for control of CiLV are a good choice for part of the integrated control of B. phoenicis. Predatory mites are considered the most efficient natural enemies of phytophagous mites. Citrus mite predators are frequently found associated with Brevipalpus spp.; mites of the Phytoseidae family such as Euseius sp., Iphiseiodeszuluagai, Amblyseius spp. and Phytoseiulus spp. are the most important natural enemies of the mite vector B. phoenicis in citrus orchards as well as the entomopathogenic fungus Metarhizium sp. and Hirsutella thompsonii. Carvalho et al. (2008) found predatory mites (Phytoseidae and Stigmaeidae) and higher mite populations of B. phoenicis during dry periods of the year in coffee plantations in Sao Paulo, Brazil; the predatory mites Euseius citrifolius and E. concordis were the most frequent.

Alternatively, control includes the use of entomopathogenic fungi; H. thompsonii and Metarhizium anisopliae var. acridum have been reported as very promising natural enemies for B. phoenicis mite control (Magalhaes and Rodriguez, 2005). Rossi-Zalaf and Alves (2006) recorded H. thompsonii as the most virulent entomopathogen for red flat mite control.

Other control alternatives

Recently, it was shown that a bacterial endosymbiont of the genus Cardinium blocks production of androgenic hormones in the early stages of mite development, resulting in feminization of haploid males (Novelli et al., 2004). As a consequence, it is commonly found that less than 1% of the population is male. Cobalt 60 irradiation to treat the bacteria Cardinium sp. influences the oviposition period and the number of eggs laid by irradiated females (Novelli et al., 2008).

Tangor Murcot, the most common Tangor variety produced in Brazil, can host CiLV-C and be asymptomatic (Bastianel et al., 2004). Genetic improvement shows that the segregation of the disease phenotype in a population obtained by crossing the F1 sweet orange variety Pera and Tangor Murcot, pathogen susceptible and resistant, respectively, suggests that some genes are involved in resistance to Citrus leprosis virus (Salvo, 1977; Bastianel et al., 2006).

Similarly, the progress achieved with the molecular genome decoding of the CiLV-C virus may result in the creation of transgenic plants with virus resistance. Researchers believe that the use of these transgenic plants in the near future will result in the suspension of acaricide applicationss to control the vector of the leprosis virus (Pascon et al., 2006).

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Organizations

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USA: University of Florida - Citrus Research and Education Center, 700 Experiment Station Rd, Lake Alfred, FL 33850

USA: USDA-APHIS (Animal and Plant Health Inspection Service), US Department of Agriculture 1400, Independence Ave., SW Washington, DC 20250, Washington, DC, USA, http://www.aphis.usda.gov/

Brazil: Centro de Citricultura Sylvio Moreira, Rodovia Anhangüera, km 158 - Caixa Postal 04, 13490-970 Cordeirópolis (SP)

Brazil: Fundo de Defensa da Citricultura, Av. Adhemar Pereira de Barros, 201 | CEP: 14807-040, Vila Melhado - Araraquara - São Paulo

Contributors

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15/07/13 Review by:

Guillermo León M, Km. 17 via Pto. López. CORPOICA C.I. La Libertad. Villavicencio, Colombia.

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