Invasive Species Compendium

Detailed coverage of invasive species threatening livelihoods and the environment worldwide

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Pseudocercospora ulei
(South American leaf blight of rubber (SALB))

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Datasheet

Pseudocercospora ulei (South American leaf blight of rubber (SALB))

Summary

  • Last modified
  • 23 September 2020
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Pseudocercospora ulei
  • Preferred Common Name
  • South American leaf blight of rubber (SALB)
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Fungi
  •     Phylum: Ascomycota
  •       Subphylum: Pezizomycotina
  •         Class: Dothideomycetes
  • Summary of Invasiveness
  • The invasive potential of SALB has been illustrated by the devastating impact that it has had on attempts to develop rubber production in the Americas. Rapid epidemic development of the disease under humid conditions can destroy young rubber plant...

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Identity

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Preferred Scientific Name

  • Pseudocercospora ulei (Henn.) Hora Júnior & Mizubuti

Preferred Common Name

  • South American leaf blight of rubber (SALB)

Other Scientific Names

  • ?Passalora heveae Massee (nom. nud.) sensu Stahel
  • Aposphaeria ulei Henn.
  • Dothidella ulei Henn.
  • Fusicladium heveae K. Schub. & U. Braun
  • Fusicladium macrosporum J. Küyper, homonym (non F. macrosporium Bonord.)
  • Melanopsammopsis ulei (Henn.) Stahel
  • Microcyclus ulei (Henn.) Arx

International Common Names

  • Spanish: enfermedad sudamericana de hoja del cauchero
  • French: flétrissure sudamericaine des feuilles de l'hévéa; maladie des feuilles sud américaine

Local Common Names

  • Brazil: mal das folhas
  • Germany: südamerikanischen battfallkrankheit
  • Indonesia: Amerika selatan
  • Netherlands: zuid-amerikaanse bladziekte

EPPO code

  • MICCUL

Summary of Invasiveness

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The invasive potential of SALB has been illustrated by the devastating impact that it has had on attempts to develop rubber production in the Americas. Rapid epidemic development of the disease under humid conditions can destroy young rubber plants. Control methods are expensive and reduce the economic value of the crop. The disease poses a major threat to the large rubber producing areas in West Africa and South-East Asia (Edathil, 1986), where strict quarantine measures are enforced to prevent entry of the pathogen (Jayasinghe, 1998; FAO, 2011).

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Fungi
  •         Phylum: Ascomycota
  •             Subphylum: Pezizomycotina
  •                 Class: Dothideomycetes
  •                     Subclass: Dothideomycetidae
  •                         Order: Capnodiales
  •                             Family: Mycosphaerellaceae
  •                                 Genus: Pseudocercospora
  •                                     Species: Pseudocercospora ulei

Notes on Taxonomy and Nomenclature

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South American leaf blight (SALB) was first mentioned by Hennings (1904), who briefly described the fungi associated with infected leaves from native rubber trees collected by Ernst Heinrich Ule at the Juruá River, Brazil in 1901 and near Iquitos, Peru in 1902. He named two new species on the material; the sexual morph as Dothidella ulei; and the purported pycnidial asexual morph as Aposphaeria ulei. Kuyper (1911) reported the disease in Suriname and subsequently described the conidial asexual morph as Fusicladium macrosporum (Kuyper, 1912): the cause of a serious disease in rubber nurseries and plantations (Rands, 1924; Holliday, 1970). Thus, at this period, all the morphs of SALB were considered to be three different species associated with diseased rubber from various countries in South America.

Massee, in 1913, independently and erroneously named the conidial form as Passalora heveae, but with no description, after material was sent to him from Guyana by Bancroft (1913),  but it was Petch  (1914) who first concluded that D. ulei, A. ulei and F. macrosporum were all forms of the same pathogen. Stahel (1917) erected the new genus Melanopsammopsis to accommodate Dothidella ulei. Later, Arx transferred it to the genus Microcyclus (in Müller and Arx, 1962; see Holliday, 1970; Evans, 2002).

Until recently, the sexual stage was named Microcyclus ulei (Henn.) Arx, the conidial asexual stage was Fusicladium heveae K. Schub. & U. Braun (in Crous and Braun, 2003) and the purported pycnidial asexual stage was Aposphaeria ulei Henn. However, under the classification system at that time, this meant that each morph or stage in the life-cycle belonged to a different ascomycete family: Planistromellaceae (Microcyclus); Venturiaceae (Fusicladium); Lophiostomataceae (Aposphaeria). This anomaly was highlighted by Evans (2002) and, subsequently, by Wingfield et al. (2011) who recommended that a single unifying generic name should be adopted in accordance with the new nomenclatural rules of the one fungus: one name system. Based on multi-gene phylogeny analyses, all morphs were proven to cluster in one species within the Pseudocercospora sensu stricto clade and, in accordance with the International Code of Nomenclature for algae, fungi and plants (ICN), the new combination Pseudocercospora ulei (Henn.) Hora Júnior & Mizubuti, was introduced (Hora Júnior et al., 2014). This is now the ratified and single unifying name for the causal agent of SALB (see taxonomic websites: Index Fungorum; MycoBank). The new phylogenetics show that P. ulei sits close to P. fijiensis – the causal agent of black Sigatoka, the most economically-damaging disease of banana – which, hopefully, will now permit the adoption of comparative epidemiological and genomic approaches, using these better-studied species of Pseudocercospora (Hora Júnior et al., 2014).

Description

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The asexual stage or morph of P. ulei is characterized by amphigenous, simple, erect, straight or slightly flexuous to geniculate conidiophores, 30-60 x 4-7 µm; mostly reduced to conidiogenous cells. Conidiogenous cells, holoblastic, integrated, cylindrical to subcylindrical, terminal, proliferating sympodially, with 1-3 loci, 2 µm diameter, flat, unthickened, not darkened. Conidia solitary, obclavate, straight to curved or twisted into a sigmoid shape, 28-60 x 6-11 µm, apex rounded, base attenuated to a truncate hilum, 0-1-septate, constricted at the septum, subhyaline to pale brown, smooth to slightly roughened, thin-walled.  

Spermogonial stage, within ascostromata; spermogonia adaxial, superficial, in groups, globose, 110-140 x 90-150 µm, walls of pale to dark brown textura angularis, 4-8 cells thick, ostiolate, smooth; spermatiophores phialidic, lageniform, integrated, 10-16 x 1-2 µm, hyaline, smooth; spermatia dumb-bell shaped, 4-7 x 1 µm, aseptate, hyaline, smooth.

The sexual stage or morph has pseudothecial, superficial. epiphyllous ascomata which are 130-165 x 90-190 µm. They are produced in the inner part of the erumpent black, carbonaceous ascostromata, 200-500 µm diameter with a rugose external wall and an inner wall of brown textura angularis, smooth, 40-60 µm diameter. Dehiscence ostiolate; asci bitunicate, clavate, 65-90 x 13-16 µm, 8-spored; ascospores ellipsoidal, 15-20 x 4-5 µm, 1-septate, constricted at septum, hyaline, smooth (modified from Hora Júnior et al., 2014).

Distribution

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P. ulei occurs in all original rainforest habitats of species of Hevea. This genus is restricted to the Amazon basin (Schultes, 1970; Priyadarshan and Gonçalves, 2003) - extending northwards to the Guiana Shield, including the Upper Orinoco, and southwards to Mato Grosso – where the fungus coevolved with its Hevea hosts (Guyot and Le Guen, 2018). In all other Brazilian states, as well as in Central and North America, P. ulei is an invasive alien species, catching up with its host wherever it has been grown. It is important to re-emphasize that SALB does not occur in Asia and Africa, which account for about 99% of the worldwide production of natural rubber.

P. ulei can be classed as invasive within its native range because of its destructive capacity in rubber plantations in the Amazon basin.

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.

Last updated: 30 Jun 2021
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Asia

SingaporeAbsent, Confirmed absent by survey

North America

BelizePresentIntroducedInvasive
Costa RicaPresentIntroducedInvasive
El SalvadorPresentIntroducedInvasive
GuatemalaPresentIntroducedInvasive
HaitiPresentIntroducedInvasive
HondurasPresentIntroducedInvasive
MexicoPresent, LocalizedIntroducedInvasive
NicaraguaPresentIntroducedInvasive
PanamaPresentIntroducedInvasive
Trinidad and TobagoPresentIntroducedInvasive

South America

BoliviaPresentNativeInvasive
BrazilPresent, Localized
-AcrePresent, WidespreadNativeInvasive
-AmapaPresent, WidespreadNativeInvasive
-AmazonasPresent, WidespreadNativeInvasive
-BahiaPresentIntroducedInvasive
-Espirito SantoPresent, WidespreadIntroducedInvasive
-GoiasPresent, WidespreadIntroducedInvasive
-MaranhaoPresent, WidespreadIntroducedInvasive
-Mato GrossoPresent, WidespreadNativeInvasive
-Mato Grosso do SulPresent, WidespreadIntroducedInvasive
-Minas GeraisPresent, WidespreadIntroducedInvasive
-ParaPresent, WidespreadNativeInvasive
-ParanaPresent, Few occurrencesIntroducedInvasive
-PernambucoPresentIntroducedInvasive
-Rio de JaneiroPresent, WidespreadIntroducedInvasive
-RondoniaPresent, WidespreadNativeInvasive
-RoraimaPresent, WidespreadNativeInvasive
-Sao PauloPresentIntroducedInvasive
ColombiaPresentNativeInvasive
EcuadorPresentNativeInvasive
French GuianaPresentNativeInvasive
GuyanaPresentNativeInvasive
PeruPresentNativeInvasive
SurinamePresentNativeInvasive
VenezuelaPresentNativeInvasive

History of Introduction and Spread

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P. ulei has prevented the large-scale commercial cultivation of rubber in South, North and Central America. Wherever new plantings were established the disease soon became epidemic and caused the collapse of the enterprise. The pathogen is native throughout the Amazonian region on indigenous Hevea species. Man may have aided distribution to other regions and countries in the Americas wherever rubber was cultivated as an exotic crop, through transport of infected planting material (Hilton, 1955; Carefoot and Sprott, 1969). Natural, long-distance dispersal of ascospores has also been suggested (Guyot and Le Guen, 2018). Apart from the record in Haiti, there has been no spread outside South, North and Central America and strict quarantine practices are aimed to exclude it from Asia and Africa (FAO, 2011).

Risk of Introduction

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RISK CRITERIA CATEGORY

ECONOMIC IMPORTANCE High
DISTRIBUTION Central & South America
SEEDBORNE INCIDENCE Not recorded
SEED TRANSMITTED Not recorded
SEED TREATMENT None

OVERALL RISK High


Notes on phytosanitary risk

A quarantine law has been established for international air travel in Malaysia because the rapid development of direct air flight connections between tropical countries is enhancing the possibility of the spread of P. ulei: passage from South American countries to Malaysia is prohibited (Anon., 1986; ASEAN, 2018). All rubber plants derived from the original collections of Henry Wickham in the Santarem region of the Brazilian Amazon in the 1870s and used in South-East Asian and African countries (Hilton, 1955; Davis, 2007) have, so far, proved to be highly susceptible to P. ulei (Chee, 1976c). Therefore, a main aim of Asian and African countries is the pro-active development of quarantine protocols, as well as control and eradication methods (Anon., 1986).These involve strict phytosanitary measures – such as, fumigation of goods and travellers arriving from South America and treatment of imported Hevea germplasm in an approved intermediate quarantine facility – as well as an emergency action programme should SALB ever arrive; including complete defoliation of rubber trees in and around 500 m of the outbreak using herbicides followed by the application of fungicides. An updated document containing a pest-risk analysis, guidelines for protection against SALB and contingency plans should it arrive has been prepared by FAO under the Asia and Pacific Plant Protection Agreement (FAO, 2011).

The deliberate introduction of SALB into disease-free areas, such as South-East Asia, should also be considered in any risk analysis and this aspect of agro- or bio-terrorism, for financial or political gain, has been highlighted recently (Onokpise and Louime, 2012). Needless to say, the impact on the global economy would be catastrophic.

Hosts/Species Affected

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P. ulei infects Hevea brasiliensis, H. benthamiana, H. camargoana, H. camporum, H. colina, H. confusa, H. guianensis, H. lutea, H. paludosa, H. pauciflora, H. randiana and H. spruceana, and hybrids between these species (Farr and Rossmann, 2013; Hora Júnior et al., 2014).

Host Plants and Other Plants Affected

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Plant nameFamilyContextReferences
Hevea brasiliensis (rubber)EuphorbiaceaeMain

Growth Stages

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Seedling stage, Vegetative growing stage

Symptoms

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The symptoms vary with the age of the infected leaves. In young leaves of susceptible clones up to 10 days of age, 3-4 days after inoculation, slightly discoloured, hypertrophic deformations are visible. 5-6 days after inoculation, greyish to olive-green masses of conidia are present on the lower leaf surface. When infection density is high, these spore-producing lesions coalesce, the leaves turn reddish and premature leaf fall is observed. The petioles, young twigs and young fruits of susceptible clones can also be infected. When conditions are favourable for disease development and in highly susceptible clones, infection and rapid re-infection of young leaflets can cause successive defoliations which lead to dieback of terminal twigs and branches and ultimately to death of young trees.

In young leaves that are older than 12-15 days, the lesions become smaller, only slightly hypertrophic and conidial production is low or even absent. In slightly infected young leaves or infected older leaves, no premature leaf fall is induced, instead, on the upper surface of these leaves, black stromatic areas form. The stromata contain spermogonial cavities in which spermatia are formed. Later on, the stromatic areas coalesce to form ring-like structures. The leaf tissue within the rings often disintegrates, creating small holes (‘shot-hole’ symptoms) within the rings. In these older parts of the stroma, ascospores are formed in pseudothecia. (See also Gasparotto and Ferreira, 1989; Hora Júnior et al., 2014).

List of Symptoms/Signs

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SignLife StagesType
Fruit / lesions: black or brown
Leaves / abnormal colours
Leaves / abnormal forms
Leaves / abnormal leaf fall
Leaves / necrotic areas
Stems / canker on woody stem
Stems / dieback
Stems / discoloration of bark

Biology and Ecology

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Transmission

The spores of P. ulei are disseminated by rain or by wind. Wind is a particularly important factor for distribution of spores within a plantation or from one area to another. Dissemination of conidia occurs mainly between 09.00 and 14.00 h, when temperature is high and relative humidity is at its lowest point. Ascospores are disseminated in the night, with a peak between 06.00 and 08.00 h (Holliday, 1969; Chee, 1976b; Rocha and Vasconcelos Filho, 1978). According to Holliday (1970) and Chee (1976a), the ascospores are liberated when leaves containing stromata are wetted and kept in the dark at 13-16°C; according to Guyot and Eveno (2015), 6-month-old ascostromata still contain viable ascospores and 80% of these can be released 30 minutes after wetting.

Disease Cycle

P. ulei infects young leaflets, those up to 12 days old being most susceptible, but thereafter becoming increasingly resistant. Lesions appear about 4-10 days after infection, on which conidia are produced and young diseased leaves are often shed. Severe conidial infections, which cause fall of young leaflets and increase the quantity of conidial inoculum, are known as the 'exploding phase' of the disease. This is the most important phase of SALB and leads to the physiological debilitation of the trees. Older leaflets that become infected do not suffer premature fall and remain on the tree. 30-60 days after infection, they develop black stromata ('sandpaper' symptoms) on which the spermogonial phase of the pathogen develops followed by the sexual, ascospore stage. According to Holliday (1970), the purported pycnidiospores germinate but do not cause any infection and this was also reported by Guyot and Le Guen (2018). Earlier, however, and in sharp contrast, Langford (1945) had reported the failure of these spores to germinate and thus to infect rubber leaves. This was confirmed by Hora Júnior et al. (2014) who posited that these are not infective spores but spermatia or mating spores, produced in spermogonia rather than asexual pycnidia, and are involved in the initial stages of the sexual cycle. The function of these spores as male gametes in plasmogamy – first suggested by Edathil (1986) – has now been accepted (Guyot and Le Guen, 2018).

After they have reached 4 or 5 years of age, rubber trees change their leaves. Ripe diseased leaves with 'sandpaper' symptoms, whether on the ground or still on the plants, provide ascospores as the primary source of inoculum. These are spread by wind and reach the young leaflets, where they germinate, penetrate and colonize the tissue. Under favourable conditions for the disease, within 5 or 6 days, the infected leaflets reveal lesions covered with conidia that may also be spread by wind or rain. Conidia are thus a secondary source of inoculum. Stromata formation takes 2 months; it then takes 1 month for asci to form and 1 month for them to mature and to liberate the ascospores. The complete life-cycle thus takes 4 or 5 months. The stromatic ascogenous stage persists on mature diseased leaves and provides the survival stage of the fungus: see Hora Júnior et al. (2014) for the hypothetical life-cycle of P. ulei; re-published in Guyot and Le Guen (2018).

The occurrence of the sexual phase enables substantial variability within the pathogen populations that has facilitated the development of new pathotypes able to overcome any host resistance that has so far been used to attempt control of the disease. Rivano (1997a) demonstrated the presence of seven virulence factors and 12 physiologic races in a collection of 16 pathogen isolates tested against 10 differential rubber clones. Lieberei (2007) identified almost 70 physiological races of P. ulei.

Epidemiology

Young rubber trees (of up to 3 or 4 years) in freshly established plantations, seed gardens and clone gardens, produce new leaves throughout the whole year. Plants that are older than 4-5 years normally change leaves once a year with the onset of the dry season ('wintering'). This leaf change behaviour is highly important for epidemics of P. ulei, because leaves are only susceptible in their growth phase up to 10-15 days. Mature leaves are completely resistant to P. ulei. The defoliation of successive flushes of new leaves severely debilitates the trees, causing dieback with curtailment of latex production; young trees may be killed.

Infections with P. ulei occur when leaves are wet. Estimates of the period of leaf wetness needed for infection vary. Rands (1924) reported that the pathogen needs 10-12 hours of free water on the leaves for infection. Langford (1945) and Hilton (1955) stated that 8 hours of free water are sufficient for successful infection. Kajornchaiyakul et al. (1984) and Gasparotto et al. (1989a) found that at 24°C not more than 6 hours of free water are necessary for infection. Gasparotto and Junqueira (1994) showed that an isolate of the pathogen did not need more than 3 hours of leaf wetness for infection and other isolates could infect within 4 hours. It must be assumed that the different periods needed for the pathogen to infect the leaf are related to the virulence of the isolates.

Various studies reveal that the optimum temperature for germination of spores of P. ulei is about 24°C, with total inhibition of sporulation at 20°C (Langford, 1945; Holliday, 1970; Chee, 1976a; Gasparotto et al., 1989a). However, Gasparotto and Junqueira (1994) found that some isolates of P. ulei are able to infect and produce spores at 16°C, but other isolates do not sporulate at 20°C. These differences seem to reflect physiological differences between isolates from different ecological regions.

 Rocha and Vasconcelos Filho (1978) in Bahia (Brazil) reported that relative humidity higher than 95% RH for 10 hours consecutively at least during a period of 12 nights per month provides the best conditions for the occurrence of SALB. Gasparotto et al. (1989b) analysed climatic data and disease incidence in Minas Gerais and found that the severity of leaf blight is positively correlated with leaf wetness, with periods of at least 90% RH and above the minimum temperature, and is negatively correlated with periods of 20°C or lower. Camargo (1976) also found that the median temperature lower than 20°C can be used as an indicator for climatic conditions unfavourable to the development of P. ulei.

According to Gasparotto et al. (1989b), there is no significant correlation between the severity of leaf blight and the frequency of rainfall and the total precipitation. Other parameters such as duration and intensity of rainfall must be analysed, because there may be direct and indirect factors, such as, enhancement of relative humidity and reduction of temperature caused by rain, which affect disease development. For example, in the north-east of Trinidad (annual rainfall >2500 mm) the incidence of leaf blight is less severe than in the north-west region with an annual precipitation between 1300 and 2500 mm (Chee, 1979). In Guatemala, the occurrence of leaf blight is much higher in the east region (annual precipitation 2500 mm) than in the west region (annual precipitation 3500 mm). According to Holliday (1969), rains with high intensity and especially with long duration remove spores out of the air and wash them from the leaflets. More recent analyses of the climatic conditions favourable for SALB have identified areas of high and low risk – the latter termed escape zones – in the major rubber-producing countries (Roy et al., 2017; Golbon et al., 2019).

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Hansfordia pulvinata Mycoparasite Fungi|Hyphae; Fungi|Spores

Notes on Natural Enemies

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The mycoparasite Hansfordia pulvinata occurs naturally in Brazil, especially in the Amazon region (Tavares et al., 2004). H. pulvinata grows as a hyperparasite on stromata, conidia and mycelia of P. ulei, but does not in practice reduce the inoculum density in plantations composed of clones that are susceptible to P. ulei.

Means of Movement and Dispersal

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Natural dispersal of P. ulei occurs through conidia and ascospores dispersed primarily by wind although rainfall assists spore release and daytime showers can lead to large transient increases in spore concentration in the air. Spore production is reduced during dry weather. Wind may disperse spores over large areas and diseased leaf debris containing the ascospore stage may also become airborne and be carried over shorter distances by gusting winds. Ascospores have been recorded throughout the year in rubber plantations, and are considered to be the main means of natural long-distance dispersal (Guyot et al., 2014; Guyot and Eveno, 2015).

Spores maybe carried incidentally by 'passive' vectors such as animals and man that may come into contact with diseased rubber foliage. For example, conidia of P. ulei have been recovered from various substrates, including the hands and clothing of people visiting SALB-infected areas (Anon., 1986; Zhang et al., 1986).

SALB has not been recorded as being seedborne, although fruits of the rubber tree can be infected.

Seedborne Aspects

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This pathogen has not been shown to be seedborne.

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 fungi/hyphae; fungi/spores Yes Yes Pest or symptoms usually visible to the naked eye
Fruits (inc. pods) fungi/hyphae; fungi/spores Yes Yes Pest or symptoms usually visible to the naked eye
Leaves fungi/hyphae; fungi/spores Yes Yes Pest or symptoms usually visible to the naked eye
Seedlings/Micropropagated plants fungi/hyphae; fungi/spores Yes Yes Pest or symptoms usually visible to the naked eye
Stems (above ground)/Shoots/Trunks/Branches fungi/hyphae; fungi/spores Yes Yes Pest or symptoms usually visible to the naked eye
Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
Growing medium accompanying plants
Roots
True seeds (inc. grain)
Wood

Wood Packaging

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Wood Packaging not known to carry the pest in trade/transport
Loose wood packing material
Non-wood
Processed or treated wood
Solid wood packing material with bark
Solid wood packing material without bark

Impact Summary

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CategoryImpact
Animal/plant collections None
Animal/plant products None
Biodiversity (generally) None
Crop production Negative
Environment (generally) None
Fisheries / aquaculture None
Forestry production None
Human health None
Livestock production None
Native fauna None
Native flora None
Rare/protected species None
Tourism None
Trade/international relations Negative
Transport/travel None

Impact

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SALB has been compared with other diseases of high economic importance, such as coffee rust (Hemileia vastatrix) and potato leaf blight (Phytophthora infestans) (Hilton, 1955; Agrios, 2005) which have the potential to change the political history of the world (Evans, 2002).

The main reasons that this disease threatens plantations include the rapid dissemination of spores, the high capacity for destruction and the difficulty in controlling the fungus. Premature leaf fall caused by P. ulei leads to dieback of trees and economic losses. Retardation of growth in seed orchards and in clone gardens reduces the number of rootstocks needed for budding as well as the amount of budwood from defined clones. Severely attacked defoliated seedlings cannot be budded and no buds can be collected from clone-defined plants because the bark is too hard and cannot be removed in the required manner. In mature plantations, successive attacks of P. ulei cause dieback of twigs or even death of the entire plant. Furthermore, attacked plants are easily infected by other pathogens which contribute to the rapid death of trees. Stahel (1917) observed that three successive defoliations within 6 months are sufficient to cause the death of trees of 5 to 6 years of age.

In 1913, SALB caused serious destruction in rubber plantations in Guyana (Bancroft, 1916) and led to the abandonment of rubber production in 1923 (Rands, 1924). In Suriname, one-third of a plantation of 40,000 trees, planted in 1911, was destroyed in 1918; the plantation was abandoned in 1920 and was substituted by coffee, cocoa and other crops (Rogers and Peterson, 1976). In Panamá, Goodyear established a plantation in 1935, but by 1940 it had been destroyed by P. ulei (Holliday, 1970).

In the 1920s, the USA received a concession from the Brazilian government to plant rubber trees in 1,200,000 ha of land at the margins of the Tapajós River, Pará (Gonçalves et al., 1983). Until 1928, the Ford Company planted 3500 ha of rubber in Fordlandia, but by 1933 about 25% of the plantation was dying as a result of the high occurrence of P. ulei. In 1934, the Ford Company transferred its activities to a nearby better-drained area (Belterra), planting 6570 ha with high-yielding Oriental clones. In 1941 and 1942, the occurrence of P. ulei increased significantly when the canopies of the rubber trees closed over, and in 1943 the plantations were destroyed by severe fungal attacks (Gonçalves et al., 1983) and the programme was more or less abandoned despite the fact that promising material had been developed, with the top-budding of over 2 million trees using the resistant H. spruceana (Eidt, 1953; Dean, 1987; Davis, 1997).

In Bahia (Brazil), rubber cultivation on a commercial scale started in 1952. Until 1970, 25,000 ha were planted with an estimated production of 5000 tons of dry rubber per year. It was planned to enhance the rubber production up to 25,000 tons per year in 1975 (Medeiros and Bahia, 1971), but in 1965 P. ulei caused the first severe damage to established plantations and many plantations were abandoned, especially in the area of Una.

Despite the high disease incidence in the Amazon region, and the earlier Ford Company fiasco, in 1972 a programme was started to enhance rubber tree cultivation in this area. The programme was well accepted and in 1982 about 75,000 ha of rubber plantations were established. As in all previous cases, when the rubber trees developed a closed canopy (around 5 years of age), the trees were severely attacked by SALB (and this Brazilian rubber programme (PROBOR) was stopped in 1986 (Lieberei, 2007).

The disease has, however, had a positive impact on promoting the development of the rubber industry and subsequent economic development in those parts of the world (Africa and especially Asia) where the disease does not occur.

Environmental Impact

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Destruction of rubber plantations results in changes of land use. Many abandoned areas revert back to secondary forest. The pathogen itself, being part of the native mycobiota, has had no lasting impact on the natural environment or on biodiversity.

Social Impact

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SALB had substantial social impacts on those involved in developing the rubber industry in South America and followed on from the economic aspects resulting in the loss of employment and migration of labour (Dean, 1987). See Carefoot and Sprott (1969), Davis (1997) and Money (2007) for popular accounts of the disease and its socio-economic impacts.

Diagnosis

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The fungus can be isolated using direct transfer of conidia from highly sporulating lesions of freshly collected young leaves. The conidia are placed on potato-dextrose agar and incubated at 24°C. The resulting colonies are small, globose and grey-greenish. After 10-12 days the first spores are produced. For intensive spore production, fragments of colonies are transferred to an agar (20 g/l) supplemented with 10 g sucrose, 6 g peptone, 2 g KH2PO4, 1 g MgSO4.7H2O and 1 ml of a 15% (g/v) chloramphenicol solution. After sterilization, 10 mg lysin-HCl, 0.25 mg tryptophane and 0.25 mg threonine are added. Fungal growth and heavy sporulation occur after 12 days' growth at 24°C, with three repetitions of 1 hour light (about 2000 lux) interrupted by 3 hours of dark, followed by 15 hours of dark. The light intervals are necessary for maximum spore production. The times may be changed according to the strains in culture (Junqueira et al., 1984). The addition of coconut water to the culture medium greatly increases conidia production (Mattos, 1999).

Guyot and Doaré (2010) reported on a method to isolate the fungus directly from ascospores in older leaves; making it possible to obtain strains from wild trees in the forest where ascostromata are the most common structures and the asexual stage is scarce and ephemeral.

Detection and Inspection

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Disease symptoms are easily visible in the field (see Symptoms).

Prevention and Control

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Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Introduction

The control of SALB is extremely difficult, because the plants grow up to 25 m high, the pathogen reveals a high physiological variability and, at present, there are no high-producing clones with satisfactory horizontal resistance. In the humid tropical region of the Amazon there is a chance to establish new rubber plantations using crown budding of high-producing clones with crowns of Hevea species that are resistant to P. ulei. However, it has been concluded recently (ASEAN, 2018; Guyot and Le Guen, 2018) that control measures, including breeding and agronomic practices, have not been successful, thus far: chemical methods proving to be expensive and impractical due to the necessity for repeated applications; and, breeding strategies have been ineffective due to the evolution of new races or pathotypes of P. ulei.

Host-Plant Resistance

The most efficient method of control is to use resistant productive clones, but clones with a sufficiently high resistance (race non-specific resistance) and good production have been difficult to find so far. The resistance of new selections is generally broken within a few years by the high variability of the pathogen. For example, Clone IAN 6158 was considered to be resistant up to 1990, but in 1991, after 700 ha had been planted in Amazonas state, the trees were severely attacked and the plantations were abandoned (Gasparotto et al., 1992). Promising clones have recently been selected in Sao Paulo state (de Souza et al., 2000). Rivano (1997b) found that Hevea clones from South America possessed the highest levels of resistance whereas those from Asia were most susceptible. Evaluation of resistance showed that smaller lesion size and lower sporulation were the main components and rates of accumulation of a phytoalexin, scopoletin and lignin were strongly correlated with resistance (Garcia et al., 1999); especially since scopoletin has been shown to be fungitoxic. Similarly, infected or damaged plants release cyanide (HCN) – cyanogenesis has been identified as an obligate feature of rubber trees – which may also be involved in host resistance (Lieberei, 2007).

Quantitative trait loci (QTLs) have been identified in Hevea germplasm which impart resistance to the disease (Lespinasse et al., 2000; Priyadarshan and Gonçalves, 2003). Thus far, eight QTLs with respect to resistance have been identified on seven linkage groups (Lieberei, 2007), whilst seven microsatellite markers have been characterised opening up the possibility of marker-assisted breeding (Lieberei, 2007).

Crown Budding

Budding of very productive rubber tree stems with crowns of clones of Hevea species that are resistant to P. ulei is an important control method, which was developed during the Fordlandia-Belterra era in the 1930-40s (Eidt, 1953; Hilton, 1955; Davis, 1997) especially in areas of high disease incidence such as the Amazon basin. According to Gasparotto et al. (1995), crown budding must be used as a plant management method in the humid Amazon area in order to substitute susceptible crowns totally or at least partially. In these 'mixed-crown' plantations, the plants with resistant crowns will serve as a barrier to the dispersal of inoculum and concurrently represent a favourable environment to natural enemies of both pathogens and phytophagous insects. In 'mixed-crown' plantations, the non-budded plants should consist of clones with a certain level of resistance or tolerance.

Escape Areas

Establishing plantations in 'escape areas or zones' is used to control SALB in the Americas. These areas have climatic conditions that are unfavourable to P. ulei, typically with cooler, less humid climates, but suitable for economic rubber tree growth. In various studies, escape areas have been identified in Brazil, and about 90% of rubber plantations are located in these zones, notably in the states of São Paulo, Mato Grosso and Espírito Santo (Camargo, 1976).

In escape areas it is necessary to search for adapted clones that change their leaves in a very short period and only during conditions which are unfavourable to the pathogen. When leaf fall occurs two times per year or in the 'wrong' weather conditions the disease will be favoured.

More recently, climatic risk analysis has been used to establish the threat posed to other rubber-producing countries by SALB, as well as to identify potential escape zones (Roy et al., 2017; Golbon et al., 2019). 

Chemical Control

Fungicides used against P. ulei include benomyl, bitertanol, carbendazim, chlorothalonil, fenarimol, mancozeb, propiconazole, thiophanate-methyl, triadimefon, triadimenol, triforine, fenbuconazole and myclobutanil (Gasparotto et al., 1990; Santos and Pereira, 1991). An evaluation of over 40 fungicides in vitro and in the field showed that only thiophanate-methyl and benomyl had any significant impact on the disease; mainly by reducing conidial production (Chee, 2008); although earlier reports from southern Bahia (Brazil) concluded that these fungicides failed to give satisfactory control in nurseries (Santos and Pereira, 1985) and this could be due to the presence of fungicide resistant strains (Hashim, 1988).

In seed gardens, clonal gardens and young developing plantations, terrestrial sprayers, tractor-mounted pneumatic sprayers or atomizers can be used. Chemical control is difficult, however, in productive rubber plantations: the trees are up to 25 m high and conventional spraying equipment does not reach the canopy. Aerial spraying, used in south-east Bahia (Brazil), is extremely expensive and not economically feasible for smallholdings and medium-sized plantations, especially when the plantations are dispersed and at far distances from one another, as found in the Amazon. Thermal fogging, though effective in Malaysia against local fungal diseases (Lim, 1982), was abandoned in Brazil, due to unsatisfactory results when applied on a commercial scale against P. ulei (Albuquerque et al., 1988).


The time and equipment used for fungicide application depends on the developmental stage of the plants and the plantations. In seed gardens and clonal gardens in areas of high disease occurrence, spraying must be done weekly in the rainy season and at 2-weekly intervals during the dry season. In plantations, spraying must be done during the refoliation or multiple-leaf-flush period at weekly intervals, until the leaves reach their mature state.  However, in older plantations it is difficult to achieve cover of the canopy using normal spraying equipment.

The effect of various techniques, including the use of sterilants, UV, heat and X-rays, on the viability of conidia has been studied in relation to the risk of spores being carried in transit on passive vectors (LebaiJuri et al., 1997).

Biological Control

The mycoparasite Dicyma pulvinata – now re-classified as Hansfordia pulvinata (see Index Fungorum; MycoBank; Wu et al., 2015) - is found colonising  the stromata of P. ulei. Application of H. pulvinata spores to highly susceptible monoclonal plantations did not lead to disease control (Junqueira and Gasparotto, 1991) but the fungus may serve as an important component in systems of integrated control and has been evaluated for potential commercial use (Bettiol, 1996). However, there is no evidence that a product based on this fungus has been marketed in Brazil, as evidenced by later studies still investigating methods of mass production (Melo and de Melo, 2009). Promising results have been achieved with crude conidial preparations in the field giving comparable control to the systemic fungicide benomyl (Delmadi et al., 2009). Characterisation of a range of Brazilian isolates of H. pulvinata from SALB outbreaks showed them to cluster together but distinct from those parasitizing other plant pathogens from different continents, indicating that this may be a species complex.

A promising new approach involves the potential use of endophytic fungi – particularly those of the genus Trichoderma - isolated from wild rubber trees in the Amazon basin in order to protect plantation trees from infection (Gazis and Chaverri, 2010; Vaz et al., 2018). Direct antagonism or indirect induced host resistance are possible mechanisms by which endophytic fungi protect their plant hosts from attack by pathogens. Preliminary results show that these fungi produce secondary metabolites active against P. ulei (Rocha et al., 2011).

References

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Distribution References

Alandia S, Bell FH, 1957. Diseases of warm climate crops in Bolivia. In: FAO Plant Protection Bulletin, 5 172-173.

Bancroft C K, 1913. A leaf disease of Para rubber. Journal Board Agricultural British Guiana. 37-38.

Batista A C, 1947. [English title not available]. (Principais doentas de plantas, no Nordeste.). Boletim de Agricultura, Pernambuco. 5-16.

CABI, Undated. CABI Compendium: Status as determined by CABI editor. Wallingford, UK: CABI

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Gasparotto L, Ferreira FA, Lima MIPM, Pereira JCR, Santos AF, 1990. (Enfermidades da seringueira no Brasil)., Manaus-AM, Brazil: EMBRAPA/CPAA.

Hennings P, 1904. On the already known parasitic fungi of Hevea species. (Uber die auf Hevea-Arten bisher beobachteten parasitischen Pilze.). Notizblatt Botanischen Gartens und Museums zu Berlin. 133-138.

Holliday P, 1970. South American leaf blight (Microcyclus ulei) of Hevea brasiliensis. In: Phytopathological Papers, Kew, Surrey, UK: Commonwealth Mycological Institute. 31 pp.

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Lamont N, Freeman W G, Warner A, Rogers C S, 1917. Rubber cultivation in Trinidad and Tobago. Bulletin of the Department of Agriculture Trinidad and Tobago. 95-152.

Langford MH, 1953. Hevea diseases of the Amazon Valley., Belém-PA, Brazil: IAN.

MARTIN W J, 1948. The occurrence of South American leaf blight of Hevea Rubber trees in Mexico. Phytopathology. 38 (2), 157-158 pp.

RANDS R D, POLHAMUS L G, 1955. Progress report on the cooperative hevea rubber development program in Latin America. Circular. United States Department of Agriculture. 79 pp.

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31/07/19 Update by:

Harry Evans, CABI-UK, Egham, UK

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