Invasive Species Compendium

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Datasheet

Moniliophthora roreri
(frosty pod rot)

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Datasheet

Moniliophthora roreri (frosty pod rot)

Summary

  • Last modified
  • 20 November 2019
  • Datasheet Type(s)
  • Invasive Species
  • Pest
  • Preferred Scientific Name
  • Moniliophthora roreri
  • Preferred Common Name
  • frosty pod rot
  • Taxonomic Tree
  • Domain: Eukaryota
  •   Kingdom: Fungi
  •     Phylum: Basidiomycota
  •       Subphylum: Agaricomycotina
  •         Class: Agaricomycetes
  • Summary of Invasiveness
  • The invasive basidiomycete pathogen M. roreri originated in Western Colombia/Ecuador. In recent years it has expanded its range in South America (Peru, Venezuela and Bolivia) and throughout Mesoamerica as far...

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Pictures

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PictureTitleCaptionCopyright
Cocoa pod infected at the young or cherelle stage, showing gross distortion due to hypertrophy and hyperplasia of internal tissues; ca. 4 weeks after infection.
TitleCocoa pod infected at the cherelle stage
CaptionCocoa pod infected at the young or cherelle stage, showing gross distortion due to hypertrophy and hyperplasia of internal tissues; ca. 4 weeks after infection.
Copyright©CABI/Harry C. Evans
Cocoa pod infected at the young or cherelle stage, showing gross distortion due to hypertrophy and hyperplasia of internal tissues; ca. 4 weeks after infection.
Cocoa pod infected at the cherelle stageCocoa pod infected at the young or cherelle stage, showing gross distortion due to hypertrophy and hyperplasia of internal tissues; ca. 4 weeks after infection.©CABI/Harry C. Evans
Irregular, chocolate-brown necrosis appearing on swollen or distorted cocoa pod ca 6-8 weeks after infection.
TitlePod 6-8 weeks after infection
CaptionIrregular, chocolate-brown necrosis appearing on swollen or distorted cocoa pod ca 6-8 weeks after infection.
Copyright©CABI/Harry C. Evans
Irregular, chocolate-brown necrosis appearing on swollen or distorted cocoa pod ca 6-8 weeks after infection.
Pod 6-8 weeks after infectionIrregular, chocolate-brown necrosis appearing on swollen or distorted cocoa pod ca 6-8 weeks after infection.©CABI/Harry C. Evans
White pseudostroma developing on dark-brown, necrotic lesion on 4- to 5-month-old cocoa pod, imparting a frosted appearance; infected at 2-3 months of age.
TitleNecrotic lesion on 4-5-month-old pod
CaptionWhite pseudostroma developing on dark-brown, necrotic lesion on 4- to 5-month-old cocoa pod, imparting a frosted appearance; infected at 2-3 months of age.
Copyright©CABI/Harry C. Evans
White pseudostroma developing on dark-brown, necrotic lesion on 4- to 5-month-old cocoa pod, imparting a frosted appearance; infected at 2-3 months of age.
Necrotic lesion on 4-5-month-old podWhite pseudostroma developing on dark-brown, necrotic lesion on 4- to 5-month-old cocoa pod, imparting a frosted appearance; infected at 2-3 months of age.©CABI/Harry C. Evans
Brown, powdery spores developing on pseudostroma on maturing cocoa pod; infected 2-3 months previously.
TitlePod infected 2-3 months previously
CaptionBrown, powdery spores developing on pseudostroma on maturing cocoa pod; infected 2-3 months previously.
Copyright©CABI/Harry C. Evans
Brown, powdery spores developing on pseudostroma on maturing cocoa pod; infected 2-3 months previously.
Pod infected 2-3 months previouslyBrown, powdery spores developing on pseudostroma on maturing cocoa pod; infected 2-3 months previously.©CABI/Harry C. Evans
Internal symptoms in a cocoa pod with no external symptoms apart from irregular, premature ripening.  Note compacted, mucilaginous bean mass.
TitleInternal symptoms in a cocoa pod
CaptionInternal symptoms in a cocoa pod with no external symptoms apart from irregular, premature ripening. Note compacted, mucilaginous bean mass.
Copyright©CABI/Harry C. Evans
Internal symptoms in a cocoa pod with no external symptoms apart from irregular, premature ripening.  Note compacted, mucilaginous bean mass.
Internal symptoms in a cocoa podInternal symptoms in a cocoa pod with no external symptoms apart from irregular, premature ripening. Note compacted, mucilaginous bean mass.©CABI/Harry C. Evans
Mature, 'healthy' cocoa pod sent from Ecuador for breeding programme; received in UK quarantine, opened to reveal internal necrosis, and left for 5 days to allow for development of pseudostroma and spores.
TitleInternal necrosis
CaptionMature, 'healthy' cocoa pod sent from Ecuador for breeding programme; received in UK quarantine, opened to reveal internal necrosis, and left for 5 days to allow for development of pseudostroma and spores.
Copyright©CABI/Harry C. Evans
Mature, 'healthy' cocoa pod sent from Ecuador for breeding programme; received in UK quarantine, opened to reveal internal necrosis, and left for 5 days to allow for development of pseudostroma and spores.
Internal necrosisMature, 'healthy' cocoa pod sent from Ecuador for breeding programme; received in UK quarantine, opened to reveal internal necrosis, and left for 5 days to allow for development of pseudostroma and spores.©CABI/Harry C. Evans
M. roreri in culture; 4 weeks on potato dextrose agar.
TitleCulture plate
CaptionM. roreri in culture; 4 weeks on potato dextrose agar.
Copyright©CABI/Harry C. Evans
M. roreri in culture; 4 weeks on potato dextrose agar.
Culture plateM. roreri in culture; 4 weeks on potato dextrose agar.©CABI/Harry C. Evans
M. roreri on wild host, Theobroma gileri, in submontane forests of north-west Ecuador.
TitleSymptoms on wild host
CaptionM. roreri on wild host, Theobroma gileri, in submontane forests of north-west Ecuador.
Copyright©CABI/Harry C. Evans
M. roreri on wild host, Theobroma gileri, in submontane forests of north-west Ecuador.
Symptoms on wild hostM. roreri on wild host, Theobroma gileri, in submontane forests of north-west Ecuador.©CABI/Harry C. Evans
Cluster of diseased pods at base of tree, showing different symptoms and signs of moniliasis: premature ripening, partial necrosis, total necrosis and creamy, mature pseudostromata.
TitleCluster of cocoa pods: various symptoms
CaptionCluster of diseased pods at base of tree, showing different symptoms and signs of moniliasis: premature ripening, partial necrosis, total necrosis and creamy, mature pseudostromata.
CopyrightLuis C. Gonzalez
Cluster of diseased pods at base of tree, showing different symptoms and signs of moniliasis: premature ripening, partial necrosis, total necrosis and creamy, mature pseudostromata.
Cluster of cocoa pods: various symptomsCluster of diseased pods at base of tree, showing different symptoms and signs of moniliasis: premature ripening, partial necrosis, total necrosis and creamy, mature pseudostromata.Luis C. Gonzalez
Total necrosis and initial mycelial growth of M. roreri on young cocoa pod.
TitleNecrosis of young cocoa pod
CaptionTotal necrosis and initial mycelial growth of M. roreri on young cocoa pod.
CopyrightLuis C. Gonzalez
Total necrosis and initial mycelial growth of M. roreri on young cocoa pod.
Necrosis of young cocoa podTotal necrosis and initial mycelial growth of M. roreri on young cocoa pod.Luis C. Gonzalez

Identity

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Preferred Scientific Name

  • Moniliophthora roreri H.C. Evans et al. (1978)

Preferred Common Name

  • frosty pod rot

Other Scientific Names

  • Monilia roreri Ciferri

International Common Names

  • English: monilia pod rot; pod rot of cocoa; Quevedo disease; watery pod rot of cocoa
  • Spanish: aguado del cacao; helada; mancha ceniza; moniliasis del cacao; podredumbre acuosa de la capsula del cacao
  • French: moniliose du cacaoyer; pourriture aqueuse de la cabosse du cacaoyer

EPPO code

  • MONPRO (Moniliophthora roreri)

Summary of Invasiveness

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The invasive basidiomycete pathogen M. roreri originated in Western Colombia/Ecuador. In recent years it has expanded its range in South America (Peru, Venezuela and Bolivia) and throughout Mesoamerica as far as Mexico. Africa, Asia and insular Caribbean are still free of this pathogen.

M. roreri causes the devastating frosty pod rot of cocoa (Theobroma cacao), a disease that commonly reduces yields by over 80% within a few years of pathogen establishment. The severe losses, and occaisionally complete crop failure, frequently render cocoa production economically unfeasible. The results are loss of livelihoods and abandonment and conversion of the affected agroforests to less environmentally sustainable uses, with secondary effects ranging from habitat loss for wildlife, fragmentation of forested landscapes and soil erosion. It is therefore imperative that the introduction of the pathogen to additional cocoa-producing regions is prevented. These include the insular Caribbean, the Guyanas and Brazil in the Americas, as well as the bulk-cocoa producing continents, Africa and Asia (Krauss, 2010).

Taxonomic Tree

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  • Domain: Eukaryota
  •     Kingdom: Fungi
  •         Phylum: Basidiomycota
  •             Subphylum: Agaricomycotina
  •                 Class: Agaricomycetes
  •                     Subclass: Agaricomycetidae
  •                         Order: Agaricales
  •                             Family: Marasmiaceae
  •                                 Genus: Moniliophthora
  •                                     Species: Moniliophthora roreri

Notes on Taxonomy and Nomenclature

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Evans et al. (1978) demonstrated the presence of dolipore septa in the vegetative mycelium, indicating Basidiomycete affinities, and on the basis of the spores in basipetal chains erected the new genus Moniliophthora, thus separating it from the acropetalous Ascomycete genus Monilia. They concluded that it represented the anamorph of an unknown Basidiomycete genus and speculated that it may be related to Crinipellis perniciosa, the causal agent of witches' broom disease of cocoa. Later, Evans (1981) posited that they represented evolutionary lines of a progenitor species. Evans et al. (2002) used cytological evidence to show that the 'conidia' are, in fact, sexual spores or meiospores, interpreted as modified basidia, which perform sexual, dispersal and resting functions. The new combination Crinipellis roreri (Ciferri) HC Evans was proposed. Molecular evidence was generated to show not only the close relationship to C. perniciosa but also that frosty pod isolates from a wild host, Theobroma gileri, in the forests of north-west Ecuador, merited separation from the cocoa isolates at the varietal level: the new variety Crinipellis roreri (Ciferri) HC Evans var. gileri HC Evans and KA Holmes. This distinction was supported by Phillips-Mora (2003) on the basis of molecular characterization, whilst both he and Griffith (2004) used molecular data to corroborate the close relationship of the frosty pod rot and witches' broom pathogens.

More recent molecular evidence (Aime and Phillips-Mora, 2005) confirms that C. perniciosa and C. roreri are sister taxa belonging to the Marasmiaceae, Agaricales. However, these two taxa form part of a distinct lineage or clade separated from the saprotrophic litter fungal genera Crinipellis and Marasmius. Moniliophthora has now been designated a teleomorph genus and the new combination M. perniciosa (Stahel) Aime has been proposed, whilst M. roreri remains with Crinipellis roreri as a synonym or non-preferred name.

The closest described relatives to the tropical Malvaceae (Sterculariaceae) pathogens M. roreri and M. perniciosa are grass endophytes that are found in the apparently healthy root cortex of Bouteloua gracilis and Sporobolus cryptandrus, sampled at several arid sites in North America, ranging from Canada to Mexico (Porras-Alfaro and Bayman, 2011). These endophytes cluster more closely with Marasmius spp. and an endophyte isolate from Yucca glauca than with Crinipellis spp. (Khidir et al., 2010). A high degree of similarity of rDNA 18S gene sequences with the genera Moniliophthora and Crinipellis was also found in a fruit rot pathogen of another Malvacea  (Bombacaceae), pochote (Ceiba aesculifolia supsp. parvifolia), in Mexico (Avendaño-Gómez et al., 2008).

Although Evans' reclassification of the fungus as M. roreri is generally accepted, Latin American plant pathologists continue to use the name 'moniliasis' to refer to the disease; a term that has been passed on to farmers by extension workers. Since the disease until recently has been present only in Spanish speaking countries, it seems reasonable to retain the widespread, though technically incorrect, term 'moniliasis' in Spanish. However, in scientific literature and English publications, it is advisable to use the common descriptive name frosty pod rot as all other cocoa disease names adhere to this rule.

Description

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The mycelium forms a 2-3 mm thick, felt-like pseudostroma on pod lesions and on solid culture media, which is covered by a dense mat of beige to tan spores which are powdery when mature. On modified V8 medium, growth rates range from 1.3 mm per day to 6.2 mm per day, while sporulation commenced after 5.0 to 13.8 days, depending on the isolate (Philips-Mora, 2003).

The mycelium is branched, septate, with basidiomycete-like dolipore septa. It forms the pseudostroma on the surface of external as well as exposed internal necrotic lesions. The hyphae are hyaline, 2-5 µm wide, slightly constricted at the septa. Sporogenous structures are either branched or unbranched, producing chains of spores which mature basipetally. On malt extract agar, spores are mostly globose (8-15 µm diameter), sometimes slightly ellipsoidal (8-20 x 5-14 µm), with thick (1-2 µm) walls (Evans et al., 1978), whereas Philips-Mora (2003) reported somewhat lower values on modified V8 medium. There, spore shape varied between isolates, with globose spores being most common (87% to 96%) in Peruvian and some Ecuadorian isolates, whereas Costa Rican and other Ecuadorian isolates had mostly (42% to 56%) ellipsoid spores (Philips-Mora, 2003).

Distribution

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M. roreri remained confined to the north-western side of the Andes in Ecuador and Colombia, eastern Panama and western Venezuela, from its discovery early in the nineteenth century until the late 1970s (Phillips-Mora, 2003 and references therein). It appeared in Costa Rica in 1978, spreading to Nicaragua and western Panama (Enríquez and Suárez, 1978) within two years. It was detected in the Amazon basin of Ecuador and Peru in the late 1980s (Silva, 1987; Hernández et al., 1990) and in Central America spread to Honduras (1997), Guatemala (2002), Belize (2004) and Mexico (2005) (Phillips-Mora et al., 2007).  In 2012, M. roreri was first detected in Alto Beni, Bolivia (Phillips-Mora et al., 2012 and in lit.). Phillips-Mora et al. (2012) cited presence in El Salvador based on a paper by Phillips-Mora and Wilkinson (2007), however this would appear invalid as there is no mention of El Salvador in the Phillips-Mora and Wilkinson paper. There is no evidence that M. roreri is present in El Salvador. 

Up to 2004 there is no official register of M. roreri's presence in the neighbouring countries of Brazil, Bolivia and Trinidad and Tobago, or in eastern Venezuela, but it may have already invaded wild populations of Theobroma and Herrania spp., or isolated cocoa plantings, in some of those countries (CABI/EPPO, 2011). By 2009, the barrier of the Andes mountains had been overcome and the pathogen was recorded in the Venezuelan states of Zulia, Táchira, Mérida, Trujillo, Barinas, Apure and Amazonas (Parra et al., 2009). The latter two, as well as parts of Barinas, are clearly located east of the Andean chain, making the expansion into Brazil and the Guyanas more likely.

As of late 2012, M. roreri remained restricted to the American tropics. Caribbean islands, with the possible exception of small off-shore islands belonging to Central American countries, were free of frosty pod rot. In 2016, M. roreri was detected and confirmed in one parish in Jamaica (IPPC, 2016, preliminary report). Occasional accounts of sightings in Africa or Asia, at least up until late 2012, were erroneous.

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: 23 Apr 2020
Continent/Country/Region Distribution Last Reported Origin First Reported Invasive Reference Notes

Africa

São Tomé and PríncipeAbsent, Invalid presence record(s)2005Island Biodiversity Race (2009)

North America

BelizePresentCABI/EPPO (2011); World Cocoa Foundation (2005); Phillips-Mora et al. (2006); EPPO (2020)
Costa RicaPresent1978InvasiveEnriquez and Suarez (1978); CABI/EPPO (2011); EPPO (2020)Present throughout suitable range
CubaAbsent, Invalid presence record(s)Krauss et al. (2010)
El SalvadorPresent, Localized2012Phillips-Mora et al. (2012)Finca la Carrera, Usulutan Department
GuatemalaPresent2002InvasiveCABI (Undated); CABI/EPPO (2011); EPPO (2020)Original citation: Phillips-Mora et al. (2007)
HondurasPresentInvasivePorras and Sánchez (1988); CABI/EPPO (2011); EPPO (2020)
JamaicaPresentJohnson et al. (2017); IPPC (2016); EPPO (2020)
MexicoPresentIntroduced2005InvasivePhillips-Mora et al. (2006a); CABI/EPPO (2011); EPPO (2020)Chiapas, Tabasco
NicaraguaPresent1980InvasiveLópez and Enríquez (1980); CABI/EPPO (2011); EPPO (2020)Present throughout suitable range
PanamaPresent1956InvasiveCABI (Undated); Miranda (1986); CABI/EPPO (2011); EPPO (2020)Present throughout suitable range; Original citation: Phillips-Mora et al. (2007)
Trinidad and TobagoAbsent, Invalid presence record(s)CABI/EPPO (2011); Krauss (2010)

South America

BoliviaPresentPhillips-Mora et al. (2012); Phillips-Mora et al. (2015); EPPO (2020)Alto Beni; established
BrazilAbsent, Never occurredEvans (1981); Anonymous (2009)Absent from cocoa-producing regions
ColombiaPresentIntroduced1817InvasivePhillips-Mora (2003); Barros N. (1977); CABI/EPPO (2011); EPPO (2020)Present throughout suitable range
EcuadorPresentIntroduced1895InvasivePhillips-Mora (2003); Suárez (1987); CABI/EPPO (2011); EPPO (2020)Present throughout suitable range
GuyanaAbsent, Invalid presence record(s)Corbin (1999)
PeruPresentIntroduced1988InvasivePhillips-Mora (2003); Hernández et al. (1990); CABI/EPPO (2011); EPPO (2020)Present throughout suitable range
VenezuelaPresent1941InvasiveCapriles de Reyes (1978); Phillips-Mora (2003); Parra et al. (2009); CABI/EPPO (2011); EPPO (2020)Zulia, Tachira, Merida, Trujillo, Barinas, Apure, Amazonas

History of Introduction and Spread

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M. roreri is believed to have evolved in the forests of western Colombia and/or Ecuador on Theobromagileri.  Early newspaper records and farmer almanacs suggest that M. roreri began devastating cocoa plantings in the Colombian Department of Norte de Santander as early as 1817 and Antioquia since the early 1850s (Phillips-Mora, 2003). The first records from Ecuador date the appearance to 1895, while the first authenticated report of the disease in Ecuador was written by J.B. Rorer in 1918 (Jorgensen, 1970 and Rorer, 1918, cited by Phillips-Mora, 2003), a century after it was first mentioned in Colombia.

The geographic spread started relatively recently, mediated by humans transporting cryptically infected cocoa germplasm (Evans et al., 2003). The pathogen expanded its range in South America (Peru, Ecuador, Venezuela, Colombia) and was first recorded in Panama (Darien Province) in 1956; from there it progressed through Central America (Costa Rica, Nicaragua, North-western Panama, Honduras) during the late 1900s. In recent years, frosty pod rot established itself in Guatemala (2002), Belize (2004), Mexico (2005) (Phillips-Mora et al., 2007), El Salvador and Bolivia (2012) (Phillips-Mora et al., 2012 and in lit.). The pathogen is almost invariably vectored by humans via the translocation of cocoa pods for planting or trade. While intent cannot be alleged, three inherent characteristics of the pathogen facilitate dissemination by ill-informed or negligent individuals: (1) exceedingly prolific sporulation, (2) the long latent (non-symptomatic) phase of approximately seven weeks and (3) the recalcitrant nature of Theobroma seeds that provokes the practice of transporting seeds in pods. The combination of these two factors has led to infected but healthy-appearing pods being discarded and subsequently giving rise to pathogen spores in new areas. Because of this false sense of security, cocoa-producing countries near the presently-known boundaries of frosty pod should exercise utmost precaution and not assume compliant behaviour, even by growers, breeders and pathologists.

Introductions

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Introduced toIntroduced fromYearReasonIntroduced byEstablished in wild throughReferencesNotes
Natural reproductionContinuous restocking
Belize 2003 Crop production (pathway cause) Yes Phillips-Mora et al. (2007) Invasive
Bolivia 2012 Crop production (pathway cause) Yes Phillips-Mora et al. (2012) Localized
Costa Rica 1978 Crop production (pathway cause) Yes Lass (1985); Phillips-Mora et al. (2007) Invasive
Ecuador 1895 Crop production (pathway cause) Yes Hernández et al. (1990); Silva (1987) May be native in wild hosts; invasive in cocoa plantings
El Salvador 2012 Crop production (pathway cause) Yes Phillips-Mora et al. (2012) Localized
Guatemala 2002 Crop production (pathway cause) Yes Phillips-Mora et al. (2007) Invasive
Honduras 1997 Crop production (pathway cause) Yes Phillips-Mora et al. (2007) Invasive
Mexico 2005 Crop production (pathway cause) Yes Phillips-Mora et al. (2007) Invasive
Nicaragua Costa Rica 1980 Crop production (pathway cause) Yes Lass (1985); Phillips-Mora et al. (2007) Invasive
Panama Colombia 1956 Crop production (pathway cause) Yes Lass (1985) Darien Province; invasive
Panama Costa Rica by 1980 Crop production (pathway cause) Yes Phillips-Mora et al. (2007); Ram (1989) Northern Panama; invasive
Peru Ecuador 1988 Crop production (pathway cause) Yes Evans et al. (1998); Hernández et al. (1990); Silva (1987) Invasive
Venezuela 1941 Crop production (pathway cause) Yes Phillips-Mora (2003) Invasive

Risk of Introduction

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RISK CRITERIA CATEGORY

ECONOMIC IMPORTANCE Globally moderate, increasing; devastating where established
DISTRIBUTION Central and South America
SEEDBORNE INCIDENCE Not recorded
SEED TRANSMITTED Not recorded

Notes on Phytosanitary Risk

A high phytosanitary risk emanates from the prolific sporulation of the pathogen. A mature pod can give rise to as many as 7 billion spores and go through multiple sporulation cycles while mummified, until virtually decomposed (Ram, 1989). Spores can be dislodged by the slightest agitation and are subsequently dispersed by wind or air currents over long distances in any weather, but dilution effects are suspected to limit to a few kilometres their practical importance in transmission to healthy trees (Porras and González, 1984). Human vectoring is the main mode of long-distance dispersal. Two factors exacerbating the risk of introduction are the long latent phase of infection on mature pods and the practice of transporting the recalcitrant seeds in pods to prevent pre-mature germination. 

M. roreri has a latent infection phase of approximately seven weeks, followed by prolific sporulation within one week of diagnostic symptom development. This leaves an extremely narrow window of opportunity for early detection. The long latent phase also conveys a false sense of security by deceiving people into believing that they are transporting healthy pods. By the time external symptoms appear, the cocoa beans inside are largely destroyed. One week after the infected pods or the shells harbouring them have been discarded, the fungus sporulates on the pod surface, releasing billions of microscopic, wind-dispersed spores into the air at the slightest agitation. Thus the transport of cocoa pods from infected areas should be prohibited and the regulation enforced diligently.

Cocoa-producing countries near the presently-known boundaries of frosty pod are well aware of the serious crop damage it will inflict in most cocoa-growing regions, and therefore maintain quarantine measures to prevent the entrance of M. roreri. The greatest concern is felt in Brazil (Silva, 1987), Trinidad (Porras and Sánchez, 1988) and the Dominican Republic (Krauss, 2010).

Habitat

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Climatic Tolerances

In the laboratory, M. roreri can grow and sporulate at temperatures ranging from 18°C to 30°C (Philips-Mora, 2003). Spore germination can take place from 10°C to 40°C. Even after exposure to 4h sunlight and temperatures of 55°C, over 60% of spores germinated when plated immediately (Ram, 1989). These temperature ranges exceed the normal growing condition for T. cacao. High humidity enhances germination, but a low percentage may still germinate at low humidity; suspected dormancy mechanisms in M. roreri are poorly understood (Evans, 1981). Drought tolerance is believed to be more limiting to the pathogen’s distribution than temperature regimes. Fungal isolates have been obtained from areas with annual precipitation of over 5500 mm and average temperatures of 26°C, as well as from areas with three to four consecutive dry months (precipitation < 100 mm per month). Thus, the climatic limitation of distribution for M. roreri is likely to be defined by the limits for its cultivated host, cocoa, as the pathogen has tolerated experimental conditions that exceeded the tolerance limits for cocoa.

The data in the climate table (see Climate) are based on this assumption as well as collection data provided by Philips-Mora (2003). Where reported extremes for cocoa globally (Wood, 1985) exceeded those for M. roreri, the former are given in parentheses.

Habitat List

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CategorySub-CategoryHabitatPresenceStatus
Terrestrial
Terrestrial – ManagedCultivated / agricultural land Principal habitat Harmful (pest or invasive)
Managed forests, plantations and orchards Principal habitat Harmful (pest or invasive)
Terrestrial ‑ Natural / Semi-naturalNatural forests Present, no further details Natural

Hosts/Species Affected

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M. roreri infects only the fruit of Theobroma and Herrania species. There is circumstantial evidence that flowers and flower cushions may harbour M. roreri, but it has never been isolated from such tissues (Evans, 1981; Ram, 1989). It has been inoculated into cocoa and other Theobroma seedlings and re-isolated from them (Evans, 1981; Ram, 1989), but no report has been found of natural infection of such tissues; it therefore does not sporulate on seedlings.

Host Plants and Other Plants Affected

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Plant nameFamilyContext
HerraniaSterculiaceaeWild host
TheobromaMalvaceaeWild host
Theobroma cacao (cocoa)MalvaceaeMain

Growth Stages

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Symptoms

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Symptoms appear only on pods, and their nature depends upon the age of the pods when infected. Pods that are infected very young <1 month) show slightly chlorotic swellings and sometimes distortion, followed by general necrosis before the pod reaches half size; the seed mass may become soft and watery.

Pods that are infected when 1-3 months old may show some swellings and/or distortion, and more generally large, necrotic, dark-brown spots with irregular borders, which grow rapidly and may cover all or part of the pod surface; larger pods show partial or total premature ripening. Necrosis spreads internally, particularly to the endocarp and placenta.

Pods that are infected after 3 months of age may show no external symptoms, or only limited necrosis, often slightly sunken, surrounded by areas of premature ripening. Infected pods are noticeably heavier than healthy ones. Internally, the endocarp, seeds and placenta may show more advanced, partial or total reddish-brown necrosis and the seed mass fails to separate from the endocarp. The pod surface remains firm in all cases.

Most of the necrotic external surface soon becomes covered by a thick, felty fungal growth (pseudostroma), at first frost-white, turning to cream, tan and then light brown. If an infected fruit is sectioned, the pseudostroma appears on the necrotic internal cut surfaces, followed by sporulation within a few days.

Infected pods remain attached to the branches and gradually shrink and dry, becoming necrotic, hard mummies, partly covered with the hardened remains of the pseudostroma.

List of Symptoms/Signs

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SignLife StagesType
Fruit / abnormal shape
Fruit / discoloration
Fruit / extensive mould
Fruit / lesions: black or brown
Fruit / lesions: on pods
Fruit / mummification
Seeds / rot

Biology and Ecology

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Associations

M. roreri is a hemi-biotroph pathogen of Theobroma and Herrania species. Reproduction in nature is not known on any other substrate, rendering M. roreri an ecologically obligate parasite.

Life Cycle

Spores germinate in a water film on cocoa pods and penetrate directly (Suárez, 1972). Spores need several hours of damp conditions to complete most infections. It then takes 3-8 weeks from infection to external symptom appearance, depending mainly on the age of the pod (Evans, 1981; Ram, 1989). Pods which are very young when infected <1 month) develop swellings and distortion in about another month, followed by total necrosis; whereas pods infected when 3 months old develop only limited internal and external necrosis 2 or 3 months later, near ripening. Pods in between undergo extensive internal and then external necrosis, reaching to part or all of the surface. External mycelium appears a few days later on those lesions, turning quickly into a frost-like, white, dense mat. Sporogenous structures are formed and sporulate profusely in a few days, the pseudostroma then turning cream-coloured from the centre outward (Suárez, 1972; Evans, 1981). M. roreri can produce up to 7 billion wind-dispersed spores over a period of nine months on a single pod remaining suspended in the canopy due to lack of phytosanitation (Evans et al., 1977).

Spore formation, release and dispersal do not require high humidity. Air currents and tree vibrations (as during harvest or pruning) release mature spores at the end of the chains in very large numbers (Evans, 1981; Porras and González, 1984; Ram, 1989).

Epidemiology

Once established in a cocoa plantation, dispersal of M. roreri from infected pods and inoculation of young pods are continuous throughout the year, their intensity depending upon climate and phenological response of the trees in each region.

High incidence of new infections occurs when heavy pod set, hot rainy weather and many sources of inoculum (infected pods with mature pseudostromata) coincide. Air-dispersed spores germinate on wet pods and penetrate in several hours, generally at night. Two to three months later a proportion of the developing pods show symptoms. The process accelerates as increasing numbers of young pods are infected, as long as flowering and fruit-set cycles prevail.

There is a positive correlation between the percentage of pods showing symptoms and rainfall occurring 3-4 months before (Evans et al., 1977; Porras and González, 1984). Temperatures in the daily range of 22-32°C favour incidence of frosty pod; at cooler temperatures the disease is less severe, as incubation periods become longer (Suárez, 1987).

In regions with a well-defined dry season, disease incidence tends to decrease as rains subside, particularly if flowering ceases. Maddison et al. (1995) suggested the selection of a suitable cultivar to take advantage of this dry season escape. Necrotic pods covered with old stroma persist as potential sources of inoculum during these periods of low disease activity, but they tend to be less effective as they age and mummify.

If infected pods are cut off from the branch and left on the ground, spores can be released from the pseudostroma for several hours, but soon become hard to blow away, and in a few days turgor changes and invasion by other microorganisms generally immobilizes spores (González et al., 1983; Aranzazu, 1988), although they retain infectivity for several weeks (Ram, 1989).

Environmental requirements

M. roreri can grow at temperatures ranging from 18°C to 30°C in the laboratory (Philips-Mora, 2003). In the wild, it is best adapted to the same environmental conditions as its obligatory hosts, Herrania and Theobroma species, i.e. the humid tropics. Thus, its geographic range is likely to be limited by the production limits for cocoa. By the same token, there is a high risk of pathogen spread to additional areas that are newly being developed for cocoa planting. 

Climate

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ClimateStatusDescriptionRemark
A - Tropical/Megathermal climate Preferred Average temp. of coolest month > 18°C, > 1500mm precipitation annually
Af - Tropical rainforest climate Preferred > 60mm precipitation per month
Am - Tropical monsoon climate Tolerated Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25]))
As - Tropical savanna climate with dry summer Tolerated < 60mm precipitation driest month (in summer) and < (100 - [total annual precipitation{mm}/25])
Aw - Tropical wet and dry savanna climate Tolerated < 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25])

Natural enemies

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Natural enemyTypeLife stagesSpecificityReferencesBiological control inBiological control on
Bacillus Antagonist not specific Sandoval et al., 1987 Colombia Cocoa
Bacillus subtilis Antagonist not specific Peralvo and Saavedra, 2006 Ecuador Cocoa
Burkholderia cepacia Antagonist not specific Peralvo and Saavedra, 2006 Ecuador Cocoa
Clonostachys byssicola Mycoparasite Hyphae not specific Bateman et al., 2005; Krauss et al., 2006b Costa Rica, Panama Cocoa
Clonostachys rosea Mycoparasite Hyphae not specific Hidalgo et al., 2003; Krauss and Soberanis, 2001; Krauss et al., 2006b Panama, Peru, Costa Rica Cocoa
Pseudomonas aeruginosa Antagonist Spores not specific Jiménez et al., 1988
Trichoderma asperellum Mycoparasite Hyphae not specific Bateman et al., 2005; Krauss and Soberanis, 2001; Krauss et al., 2006b Peru, Costa Rica, Panama Cocoa
Trichoderma harzianum Mycoparasite Hyphae not specific Ecuador Theobroma spp.
Trichoderma longipilis Mycoparasite Hyphae not specific Krauss and Soberanis, 2001 Peru Cocoa
Trichoderma ovalisporum Mycoparasite Hyphae not specific Holmes et al., 2005; Holmes et al., 2006 Ecuador, Costa Rica Cocoa
Trichoderma paucisporum not specific Samuels et al., 2006 Ecuador Cocoa
Trichoderma stromaticum Mycoparasite Hyphae not specific Krauss and Soberanis, 2002 Peru Cocoa
Trichoderma theobromicola Antagonist not specific Samuels et al., 2006 Peru Cocoa
Trichoderma virens Mycoparasite Hyphae not specific Krauss and Soberanis, 2001 Peru Cocoa

Notes on Natural Enemies

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Fungi, bacteria and nematodes may parasitize old pseudostroma, particularly on the ground (Evans, 1981; González et al., 1983; Aranzazu, 1988). Numerous microbial antagonists of M. roreri isolated from diseased pods have been proven experimentally to reduce disease incidence, particularly bacteria of the genera Bacillus and Pseudomonas (Bravo and Victoria, 1981; Jiménez et al., 1988), but none has been tested as yet on a commercial scale. Nearly 30 species of mycoparasitic fungi were isolated from frosty pod on its wild host (Theobroma gileri) in north-west Ecuador; high parasitic activity was shown by a complex of Clonostachys and Trichoderma species (Evans et al., 2003b). Members of these two genera have been field tested for their biocontrol potential (see Prevention and Control).

Means of Movement and Dispersal

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Natural dispersal occurs principally by wind. Even in the absence of wind barriers, the potential for air-borne spread is believed to be limited to a few kilometres from any single source, due to the weight of the spores as well as their susceptibility to the elements. Vectored transmission is dominated by human activity and has the potential for global spread to any area with suitable host plants (Phillips-Mora, 2003, and references therein).

Seedborne Aspects

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M. roreri is not seedborne, but the fungus can be disseminated into new geographic areas inside cocoa pods intended as seed sources, a means to keep seed viable during transport (Evans, 1981; Porras and Sánchez, 1988; Ram, 1989). Healthy-looking pods with limited internal lesions tend to be discarded after opening, and M. roreri will sporulate on such lesions; such seems to have been the case when the fungus was introduced into Costa Rica in 1978 (Enríquez and Suárez, 1978). Similarly, M. roreri spread from western Ecuador to the Aguarico and Napa valleys in eastern Ecuador following the construction of oil roads. From there, it entered Peru via the exchange of agricultural produce in fairs which, prior to border conflict, were regularly visited by farmers from both countries (Evans et al., 1998).

Pathway Causes

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CauseNotesLong DistanceLocalReferences
Crop productionDominant dispersal, accidental, associated with cocoa production Yes
Seed tradeFor cocoa production Yes
SmugglingUnregulated or non-enforced restrictions on movement of cocoa seeds and pods Yes

Pathway Vectors

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VectorNotesLong DistanceLocalReferences
GermplasmDominant dispersal associated with cocoa production Yes
Plants or parts of plantsDominant dispersal associated with movement of cocoa pods and seeds Yes
WindDominant natural means of dispersal Yes

Plant Trade

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Plant parts liable to carry the pest in trade/transportPest stagesBorne internallyBorne externallyVisibility of pest or symptoms
Fruits (inc. pods) hyphae; spores Yes Yes Pest or symptoms usually visible to the naked eye
Stems (above ground)/Shoots/Trunks/Branches spores
True seeds (inc. grain) hyphae; 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
Flowers/Inflorescences/Cones/Calyx
Growing medium accompanying plants
Leaves
Roots
Seedlings/Micropropagated plants
Wood

Impact Summary

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CategoryImpact
Cultural/amenity Negative
Economic/livelihood Negative

Impact

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Losses to the cocoa crop caused by frosty pod, in the absence of control efforts, depend on climatic conditions of each region and their relationship to crop phenology. Under continuous rainy weather (short or undefined dry season), high temperatures (20-30°C daily range or higher) and main pod-set peaks coinciding with rainy periods, losses can reach 80-90% of annual yields, as in the Atlantic region of Costa Rica (Enríquez et al., 1982; Porras and González, 1984). In regions with a well-defined dry season of 4 months or more, yield losses from frosty pod may remain around 20-30% when much of the pod-development cycle occurs in the dry season, as in the Machala region of Ecuador (Evans et al., 1977). Losses in Colombia's major cocoa regions average 30-40% over several years (Barros, 1977); overall losses in Peru have been put at 40-50%, with total loss in some areas and the subsequent abandonment of farms (Evans et al., 1998). These figures indicate a devastating impact on cocoa yields wherever M. roreri is present. The only reason M. roreri is not rated higher as a cocoa pathogen of global dimensions is its limited distribution to Latin America, i.e. absence from bulk producing regions in Africa and Asia. Should this continental barrier be breached, global cocoa supplies would be seriously threatened.

Environmental Impact

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Close to nothing is known about the ecological impact of M. roreri on its hosts in the wild. Impact studies have been conducted on cocoa (Theobroma cacao) in cultivation. Cocoa is typically produced by smallholders and is uniquely suited for cultivation in remote areas due to its relatively high value per weight and low perishability. Compared to other cash crops, cocoa is produced in an environmentally-friendly fashion; it is commonly grown in diverse agroforestry systems, under shade, thereby preventing soil erosion and maintaining watershed functions. Cocoa-based agroforestry systems also play an important role as buffer zones in the vicinity of protected areas, by protecting tropical forests and by providing a refuge for many animal and plant species, decreasing de facto fragmentation. Significance of cocoa in cultural activities and religious ceremonies has been described for several cultures far beyond the native distribution of the plant. A pathogen like M. roreri that destroys the cocoa beans will have a detrimental impact on livelihoods and traditions associated with cocoa production and trade.

Frosty pod rot causes yield losses in cocoa of up to 100%, although it does not kill the plant. In most countries, yield losses amount to around 70-80% within a few years of pathogen establishment and can soon lead to complete crop failure (Krauss et al., 2003). This frequently renders the production of cocoa, an environmentally sound understory crop in highly diverse agroforestry systems, as uneconomical and unattractive, leading to the abandonment and conversion of the affected agroforests. This, in turn, results in habitat loss for wildlife through the felling of trees and fragmentation of landscapes and also triggers unsustainable trends in livelihoods, due to the conversion of forest into cattle pasture, moves towards monocultures of annual crops, or urbanization with the concomitant real estate development. 

Risk and Impact Factors

Top of page Invasiveness
  • Proved invasive outside its native range
  • Abundant in its native range
  • Tolerates, or benefits from, cultivation, browsing pressure, mutilation, fire etc
  • Tolerant of shade
  • Highly mobile locally
  • Long lived
  • Has high reproductive potential
  • Reproduces asexually
  • Has high genetic variability
Impact outcomes
  • Damaged ecosystem services
  • Ecosystem change/ habitat alteration
  • Negatively impacts agriculture
  • Negatively impacts cultural/traditional practices
  • Negatively impacts livelihoods
  • Reduced native biodiversity
Impact mechanisms
  • Pathogenic
Likelihood of entry/control
  • Highly likely to be transported internationally accidentally
  • Highly likely to be transported internationally illegally
  • Difficult to identify/detect as a commodity contaminant
  • Difficult to identify/detect in the field
  • Difficult/costly to control

Diagnosis

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The narrow host range and combination of symptoms (see Symptoms) are sufficient to positively diagnose advanced stages of infection in the field. There is potential, however, for confusion with similar species or conditions to those unfamiliar with the disease.

For diagnosis at early stages, destructive sampling is recommended to all but those few who are sufficiently familiar with both the disease and the local cocoa cultivars to judge by subtle discolorations, deformations and unusual increase in pod density alone. The sliced pod test (Krauss et al., 2006a) is a robust method to distinguish frosty pod rot from other disorders or yield a positive result for M. roreri in pods with mixed disorders, including cherelle wilt. The sliced pod test yields clear results within 3-5 days and does not require laboratory facilities, allowing it to be carried out in remote field locations. It does, however, require destructive sampling. A less destructive alternative is to superficially slice into swellings or deformations in the exocarp of pods suspected of being infected. M. roreri produced fine black streaks or dots that can only be mistaken with lesions caused by M. perniciosa

The fungus can be easily isolated onto agar media, such as PDA, yeast extract agar or malt extract-maltose agar. The white radial growth on Petri plates at 24°C ranges from 5 to 10 cm in 2 weeks; abundant, cream to tan-coloured sporulation starts at 4-7 days in the centre.

While spores are easily obtained by blowing, tapping or gently scratching mature cream or tan pseudostromata of pods or isolated colonies, the small and transparent spores are not distinctive enough for positive identification by microscopic examination.

Detection and Inspection

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Given the devastating yield losses caused by frosty pod rot within a few years of disease establishment, growers in countries and regions free of the disease are anxious to maintain disease-free status and vigilantly reconfirm the absence of cream to tan pseudostromata on pods. Cocoa-producing countries particularly at risk of M. roreri introduction have developed measures for early detection and rapid response. The Dominican Republic, as the world’s largest producer of organic cocoa, linked its nation-wide diagnostic network with the incipient Caribbean Pest Diagnostic Network (Reyes Valentín et al., 2010). Brazil combined classical spore trapping with an enzyme-linked immunosorbent assay (ELISA) to detect the inconspicuous spores of M. roreri and distinguish them from other fungal taxa (Pomella et al., 2005). Sentinel stations near the borders with Colombia and Peru, where the disease is rife – far away from the cocoa-producing regions of Eastern Brazil – are proposed, in the hope that distant rapid response could win enough time to save the Brazilian cocoa industry from an invasion by M. roreri

Early detection and a rapid response leading to eradication have never been applied successfully against frosty pod rot. After a latent infection phase of approximately seven weeks, there is an extremely narrow window of opportunity for early detection, as prolific sporulation occurs within one week of diagnostic symptom development. Thus, Krauss (2010) recommended training farmers as well as field officers in the recognition of early symptoms of frosty pod rot and offered tools for this purpose.

Where frosty pod is established, quantitative disease assessment involves the counting and removal of all pods that can be positively identified as infected with frosty pod rot. The aforementioned sliced pod assay can give diagnostic clarity.

Similarities to Other Species/Conditions

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Moniliophthora perniciosa

Symptoms on cocoa pods infected with M. perniciosa (witches' broom disease) are identical to those with M. roreri, except that M. perniciosa does not grow or sporulate on any pod surface. Also, M. perniciosa infects vegetative tissue, causing proliferation, hypertrophy and distortion of shoots, branches and leaves, leading to necrosis and production of basidiocarps 1 cm diameter. As of 2004, witches' broom and frosty pod rot overlap in Bolivia, Colombia, Ecuador, Panamá, Peru and Venezuela. Using molecular techniques, it has been shown that these are sister species in the Basidiomycetes (Evans et al., 2003a; Griffith, 2004).

Cherelle wilt

Complete necrosis of young pods (up to 2 months of age) can be caused by M. roreri, M. perniciosa and, more frequently, by physiological factors, in the latter case being termed 'cherelle wilt'. M. roreri does not grow or sporulate on very young pods, so pod losses at this stage generally cannot be diagnosed with precision.

Phytophthora rot

Early fruit symptoms of black pod disease (caused by several Phytophthora species, most notably P. palmivora) are similar to the necrotic stages of frosty pod rot. However, black pod is not preceded by swellings or distortion, its necrosis grows faster in the exocarp than frosty pod, and sporulation is from a sparse, greyish mycelium which is much less conspicuous than M. roreri's thick, creamy pseudostromata.

Mixed infections do occur, e.g. M. perniciosa, M. roreri, and P.palmivora have all been isolated from different lesions on single pods. In such cases it is reasonable to assume Moniliophthora species to be the primary pathogens, as they, and particularly M. roreri, possess a latent phase that Phytophthora spp. are lacking.

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.

M. roreri only infects the fruit and only of two closely related genera, Theobroma and Herrania. Thus prevention can focus on prohibiting the transport of the pods, e.g. for transporting the recalcitrant seeds of these two species, whether they appear healthy or not, and enforcing this regulation effectively. However, as mentioned above, the pathogen’s latency period is deceiving and may tempt non-compliant behaviour. One key element to minimize infractions is education and training of front-liners (Krauss, 2010). However, even those with a vested interest, such as growers and researchers, do not always act consistent with their level of knowledge. Given the devastating losses frosty pod rot brings about, decision-makers are well-advised to invest in effective enforcement. 

Cultural Control and Sanitary Methods

Cultural control is the central pillar of any integrated frosty pod rot management. Diseased pods have to be removed from cocoa trees before the pathogen sporulates on these pods. The pathogen has a latent phase of approximately seven weeks; growers in frosty pod-affected countries tend to be able to recognize the disease one week before sporulation. This diagnostic capability dictates the required phytosanitation frequency, if sporulation is to be prevented. Although epidemiologically sound, weekly phytosanitation is cost-effective only in a few low-wage regions. Therefore Krauss et al. (2006a) suggested more effort in training farmers to recognise earlier stages of infection.

All diseased pods must be removed from the tree at intervals before sporulation begins. Cuts must be clean at the peduncle to avoid exposure of internal tissue, on which the fungus sporulates even after the pods are removed. Once cut off, all diseased pods can be left undisturbed on the ground, to allow for microbial inactivation of the spore mass if present (González et al., 1983; Aranzazu, 1987).  Mummified pods in the canopy can go through 10-14 sporulation cycles for up to 80 days (Ram 1989). Such spores can remain viable for up to nine months (Evans 1981), whereas pods on the ground decompose quickly and spores lose their viability.

In regions with a well-defined harvest peak and where incidence of frosty pod increases towards harvest, total pod removal (both healthy and diseased pods) at the end of the peak may be necessary to break the disease cycle (Porras and Sánchez, 1988). In any case, all mummified pods should be removed from the trees before the next flowering peak (Evans, 1981; Ram, 1989).

For effective phytosanitation, tree canopies in the plantation must be kept low and thinned by frequent light pruning, in order to provide ventilation and facilitate timely detection and removal of diseased pods (Barros, 1980; Evans, 1981; Suárez, 1987). There is no short-cut to cultural measures, including formation and maintenance pruning. Chemical and biological agents are being developed as supplementary management options (see below).   

Regulatory Control

Regions or countries free of frosty pod must maintain quarantine regulations, aimed not only at pod transport from infested areas but also related trash or residues that may harbour spores. Theobroma-free natural barriers, to break tree-to-tree dispersal, might be feasible. In-pod seed transport, as for research or breeding purposes, should require quarantine examinations in non-cocoa-growing regions. Vegetative propagation material should be dipped in fungicide suspension to prevent external transport of spores.

Internal quarantine is also possible, if some coco-producing regions in a country are free of frosty pod while others are infested.

For cultural frost pod control to be effective, phytosanitation also needs to be enforced in neighbouring plantations, as elimination of inoculum sources is useless if airborne inoculum continues coming in from nearby areas. This requires local phytosanitary regulations and can only be successful if no wild hosts of the pathogen exist in the adjacent forest, such as wild Sterculariaceae.

Chemical Control

Bateman et al. (2005) defined the criteria for selecting chemical control agents. These should (a) have low mammalian toxicity, (b) be effective against the target organism and (c) be relatively inexpensive. As early as 1979, Villegas and Enríquez reviewed the literature on fungicides effective against frosty pods rot, which, at the time, were mostly contact fungicides. Subsequently, Laker and Rudgard (1989) and Laker (1991) expanded their research to agents effective against the closely related witches’ broom disease (Crinipellis perniciosa (Stahel) Singer). Ram (1989) found the most effective compounds to be chlorothalonil, cuprous oxide and dichlofluanid. He recommended a combination of the former two, as this also killed epiphytes that interfere with flower formation. However, the toxicity of chlorothalonil renders undesirable for smallholder handling. Bateman et al. (2005) found the toxicity class III triazole fungicides bitertanol and triadimenol to be no more cost-effective than prophylactic applications of copper hydroxide, while the systemic oxathiin fungicide flutolanil may protect young pods in particular. Given the lower toxicity of copper hydroxide compared with copper oxide, the former should be preferred. Research into improved cost-effectiveness of fungicide applications via improved- targeting delivery to coca pod is in its infancy (Bateman et al., 2005; Hidalgo et al., 2003).

Biological Control

Biological control of M. roreri can be categorized into two approaches: classical and inundative biocontrol. Inundative biocontrol uses antagonists native to the area where the pathogen is to be controlled.  The argument in favour of inundative biocontrol is adaptation of the agent to local agroecological conditions. In order to achieve good control, these agents typically have to be applied in relatively large quantities and repeatedly throughout the season, which is expensive. This approach has been developed for the control of cocoa pod diseases in Peru with yield increases of up to 16.7% (Krauss and Soberanis, 2001; 2002), but proved less promising in Costa Rica (Krauss et al., 2003). There, classical biocontrol may be more applicable, as both the crop and the pathogen are removed from their centre of origin.

The classical approach is applicable in situations where a pest has been introduced into new regions. In the absence of natural enemies, the exotic pest escalates into a problem, frequently far more serious than in the country of origin. In such cases, the strategy is to introduce a coevolved, natural enemy of the pest into the new location to re-establish the natural equilibrium (Evans, 1999; Bateman et al., 2005). Establishment can be the most difficult aspect of this approach to achieve, but, if successful, the introduced agent becomes self-perpetuating. 

Evans et al. (2003b) collected numerous candidates for frosty pod rot control from Theobroma gileri in western Ecuador, most notably Clonostachys spp. and Trichoderma spp. An endophytic and mycoparasitic isolate of Trichoderma ovalisporum subsequently yielded respectable results in both Ecuador and Costa Rica (Holmes et al., 2006; Krauss et al., 2010). Endophytic biocontrol agents have been implicated in induced systemic resistance (Bailey et al., 2006). They also create a much wider window of opportunity for antagonism through exclusion (competition), mycoparasitism and/or antibiosis, because spores of M. roreri germinate and penetrate the pod surface soon after landing there to establish a systemic pod infection, which can be latent for two months (Evans, 1981). Coevolved endophytic antagonists may thus be a particularly suitable medium-term solution for the classical biocontrol of Moniliophthora spp. in cocoa planted outside their South American centre of origin (Krauss et al., 2010).

Host-Plant Resistance

There are differences in susceptibility to M. roreri in most cocoa clonal collections tested (Arangundi et al., 1988; Cárdenas et al., 1987; Jiménez et al., 1987; González and Vega, 1992). Materials mentioned in more than one test as having some resistance include cultivars IMC-67, PA-169, P-7, EET-233, UF-676, UF-296 and many of their hybrid progenies. Recent studies in Costa Rica added UF-273, UF-712, EET-75 y PA-169 to this list (Arciniega, 2005).

Modern breeding for frosty pod rot resistance focuses on horizontal resistance, which is less complete but more durable - an important consideration in a perennial crop. In Colombia, during field trials with artificial inoculation, clone ICS-95 showed consistent resistance against several isolates that belong to four genetic groups of the pathogen (Phillips-Mora et al., 2005). In Costa Rica, resistance is reported in the clones CATIE-R4 and CATIE-R6, whereas CATIE-R1 is moderately resistant, and CC-137, ICS-96 T1 and PMCT-58 are moderately susceptible to artificial inoculation with a local isolate as well as in the field (Phillips-Mora et al., 2012) Schnell et al. (2007) identified a quantitative trait marker(s) each for frosty pod rot, witches’ broom and black pod resistance, which are being used in accelerated breeding for resistance.

References

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30/11/12 Updated by:

Ulrike Krauss, Ministry of Sustainable Development, Energy, Science and Technology, Saint Lucia

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