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1650 PHYTO PATH OLOGY
Symposium
Cacao Diseases: Important Threats to Chocolate Production Worldwide
Black Pod: Diverse Pathogens with a Global Impact on Cocoa Yield
David Guest
University of Sydney, NSW 2006, Australia.
ABSTRACT
Guest, D. 2007. Black pod: Diverse pathogens with a global impact on
cocoa yield. Phytopathology 97:1650-1653.
Pathogens of the Straminipile genus Phytophthora cause significant
disease losses to global cocoa production. P. m e ga k a r y a causes signifi-
cant pod rot and losses due to canker in West Africa, whereas P. c a p sici
and P. citrophthora cause pod rots in Central and South America. The
global and highly damaging P. palmivora attacks all parts of the cocoa
tree at all stages of the growing cycle. This pathogen causes 20 to 30%
pod losses through black pod rot, and kills up to 10% of trees annually
through stem cankers. P. palmivora has a complex disease cycle involving
several sources of primary inoculum and several modes of dissemination
of secondary inoculum. This results in explosive epidemics during favor-
able environmental conditions. The spread of regional pathogens must be
prevented by effective quarantine barriers. Resistance to all these Phy-
tophthora species is typically low in commercial cocoa genotypes. Dis-
ease losses can be reduced through integrated management practices
that include pruning and shade management, leaf mulching, regular and
complete harvesting, sanitation and pod case disposal, appropriate fertil-
izer application and targeted fungicide use. Packaging these options to
improve uptake by smallholders presents a major challenge for the in-
dustry.
The Straminipile genus Phytophthora probably causes more pro-
duction losses globally than any other disease of cocoa. P. palmi-
vora has several hundred recorded hosts and is of universal im-
portance in cocoa, causing global yield losses up to 20 to 30%
and tree deaths of up to 10% annually, although individual farms
in wetter cocoa-growing areas may suffer total loss (6,7,11,20). P.
megakarya is now the most important cocoa pathogen in Central
and West Africa, frequently causing total loss of pods (11,22). It is
endemic to Equatorial Guinea, Gabon, Cameroon, Togo, Nigeria,
and Ghana, and is still in an invasive phase in neighboring Côte
d’Ivoire (16). P. capsici and P. citrophthora pod rots are common
in Central and South America and may cause significant losses
under favorable environments (7). Other species including P.
megasperma and P. k a t s u r a e have also been reported to cause pod
rots. Significantly, the two major species, P. palmivora and P.
megakarya, originated away from the centre of diversity of cocoa,
and are thus “new encounter” diseases.
Disease symptoms and pathogen biology. The most striking
symptom caused by Phytophthora spp. is pod rot or black pod
(Figs. 1 and 2). Pod lesions begin as small, hard, dark spots on
any part of the pod, at any stage of pod development. Lesions
grow rapidly covering the entire pod surface and internal tissues,
including the beans, of susceptible genotypes within a few days.
Colonized pods shrivel to form a mummified pod, which in the
case of P. palmivora provides a reservoir of inoculum for at least
3 years (4). Under humid conditions a single pod may produce up
to 4 million sporangia (containing motile zoospores) that are dis-
seminated by rain, ants, flying insects, rodents, bats, and flying
foxes; on contaminated harvesting and pruning implements; and
in contaminated soil (11). Pod rot symptoms due to P. megakarya
are very similar but symptoms appear quicker and sporulation is
usually more abundant (11,22) (Fig. 2).
P. palmivora and P. megakarya infect bark, flower cushions,
and chupons causing cankers. Cankers at the base of the trunk
may extend to the main roots. Canker lesions are hidden by the
bark but often exude a reddish gum or infect flower cushions,
killing the flowers. Scraping the surface of the bark reveals a dis-
crete spreading reddish lesion in the inner bark that usually does
not penetrate deep into the wood (Fig. 3). The significance of
Phytophthora stem canker is probably underestimated, as cankers
reduce tree vigor and pod carrying capacity, thus reducing yield.
Cankers may also provide an important source of inoculum for
pod rot (11,12). Canker development is often associated with stem
and bark borers, including the longicorn beetle (Glenea spp.) and
Pantorhytes spp., which may be attracted to them. Girdling
cankers cause the sudden death of up to 10% of trees each year,
reducing production and imposing an extra cost in replanting and
lost production as replanted trees mature.
In humid conditions, P. palmivora also causes seedling and leaf
blight. Infections of fine roots are also common, however these
appear to be more important as a source of inoculum than as a
cause of serious injury to the tree, particularly if a leaf mulch
layer is present.
Sexual reproduction requires two mating types (A1 and A2) in
the heterothallic species P. megakarya and P. palmivora, however
oospores are rarely observed in nature, possibly because opposite
mating types are rarely found together (1). There is some evi-
dence of natural hybrids where compatible mating types of
P. palmivora and P. megakarya co-exist (8). The pathogen com-
monly survives as mycelium and chlamydospores (thick-walled
resistant spores) in infected plant material, usually roots, cankers
or mummified pods (P. palmivora), or in the soil (P. megakarya)
(11).
Epidemiology. Although symptoms appear year-round, the
most severe epidemics coincide with the proliferation of sporangia
and insect vectors during the wet season. In the presence of mois-
ture, sporangia release the infective propagules, zoospores. Zoo-
spores need 20 to 30 min in free water on plant surfaces before
Corresponding author: D. Guest; E-mail address: d.guest@usyd.edu.au
*The e-Xtra lo
g
o stands for “electronic extra” and indicates that the online version
contains su
pp
lemental material not included in the
p
rint edition. Fi
g
ures 1, 2, and 3
appear in color online
doi:10.1094/ PHYTO-97-12-1650
© 2007 The American Phytopathological Society
e-Xt
r
a*
Vol. 97, No. 12, 2007 1651
they encyst, germinate, and penetrate host tissues. Under favor-
able conditions sporangia develop within 48 h of infection.
As a soilborne pathogen that infects the aerial parts of cocoa
trees, the key epidemiological question is how the pathogen
reaches into the canopy. P. palmivora survives less than 10 months
in soil as a saprophyte, depending on the ground cover (17). Rain
splash, aerosols, contaminated equipment, rodents, and ants are
potential mechanisms of inoculum movement into the canopy.
However, rain splash dispersal of P. palmivora from the soil sur-
face or piles of pod cases is limited to 75 cm, and there is little
evidence to indicate that aerosols are created under the relatively
protected canopy of cocoa trees (11). Once in the canopy, reser-
voirs of inoculum are established in cankers, in infected flower
cushions and mummified pods. However, in their detailed study in
Nigeria, Gregory and Maddison (11) concluded that when all the
known pathogen dissemination mechanisms were tallied, up to
40% of pod rot lesions resulted from “no obvious source” (11).
The recent report from Papua New Guinea that flying beetles
carry inoculum into the canopy, and especially to pods, may re-
solve the origin of infections with “no obvious source”, and re-
quires confirmation in other cocoa growing areas (18). Beetles
colonize Phytophthora lesions on pods of susceptible cultivars
more rapidly and more extensively than on less susceptible culti-
vars, and identification of the factors involved, possibly attrac-
tants in susceptible genotypes or repellents in resistant genotypes,
could be useful for breeding programs.
By contrast, the soilborne phase of P. megakarya is dominant.
Root infections maintain a reservoir of inoculum that releases zoo-
spores into the soil surface water. Zoospores spread by rain splash,
stepwise up the plant, from pods closest to the ground until the
entire tree is affected. P. megakarya does not survive in mummified
pods but remains viable in bark and sapwood for several months
and in infected debris for at least 18 months, Brasier et al. (11).
Disease management. Quarantine. Whereas P. palmivora is
globally distributed, pathogenic diversity within the species exists
and the introduction of exotic isolates poses a significant threat to
cocoa production (1,6). Efforts should be made to prevent the
movement of Phytophthora spp., particularly P. megakarya from
West Africa to other cocoa-growing regions. The movement of
soil between cocoa-growing areas must be avoided and cocoa
germplasm must be exchanged thorough intermediate quarantine
facilities (16,22).
Resistance. Breeding for resistance offers the best long-term
management strategy; however, progress incorporating durable
resistance into cultivars with desirable agronomic and quality
attributes has been slow. As a genetically variable perennial tree,
cocoa improvement presents significant challenges to breeders.
Additionally, most breeding programs have focused on yield and
quality under intense management regimes and correspondingly
low rates of disease, thus neglecting the impact of disease on
yields under smallholder farm conditions.
Amelonado-type Lower Amazon and Upper Amazon selections
appear less susceptible to Phytophthora than Trinitario and
Criollo types, and are widely used in breeding programs (15).
Reliable screening assays for resistance using detached leaves or
pods have been developed and correlate well with field observa-
tions of pod rot incidence (13,14,24). These assays are now used
in breeding programs to identify and cull highly susceptible
progenies.
Resistance to Phytophthora has been identified as additive and
polygenic (5,10) and does not appear specific for at least the two
most important species of Phytophthora, P. palmivora and
P. megakarya (21). A number of different quantitative trait loci
(QTLs) for resistance to Phytophthora have been identified in leaf
disk, pod inoculation, and field studies, although so far none of
these markers appear consistently (9). Nevertheless, with further
development and improved precision, marker assisted selection
for resistance should assist future cocoa breeding programs.
Fig. 1. Pod rot caused by Phytophthora palmivora.
Fig. 2. Pod rot caused by Phytophthora megakarya (Courtesy P. R. Tondje;
Reprinted from Bowers, J. H., Bailey, B. A., Hebbar, P. K., Sanogo, S., and
Lumsden, R. D., 2001, The impact of plant diseases on world chocolate pro-
duction, Online, Plant Health Progress, doi:10.1094/PHP-2001-0709-01-RV).
1652 PHYTO PATH OLOGY
An alternative approach to identifying resistance is to seek out
healthy individual trees among the great diversity of genotypes on
farms under high natural disease pressure. The genetic diversity
resulting from germplasm introductions over time and natural
crossing has generated stunning examples of segregation for dif-
ferent levels of susceptibility in neighboring trees (19). Once
identified and validated in genotype–environment trials, these
individuals can be used to provide budwood for farm renovation
and for inclusion in breeding programs.
Biological control. There has been extensive research into the
discovery and application of conventional inundative biological
control agents against Phytophthora diseases of cocoa. Although
there have been many reports of antagonistic and mycoparasitic
fungi inhibiting the growth of Phytophthora in vitro, no com-
mercial products have been released or widely adopted by cocoa
farmers. The short life cycle, phenomenal reproductive capacity,
complex disease cycle, and zoospore motility of Phytophthora
generates explosive epiphytotics in cocoa have so far rendered
inundative biological control agents ineffective.
The discovery and development of antagonistic endophytes of-
fers more promise. Endophytic fungi are naturally transmitted
from mature trees to seedlings in the natural cocoa forest eco-
system, however they eventually disappear from plantations. Re-
cent evidence suggests that antagonistic endophytes re-introduced
into cocoa persist and protect the tree against Phytophthora (2).
Endophytes could play an important role in integrated disease and
pest management programs.
Biological suppression and antagonism following the use of
mulches and composts improves soil health and microbial activity
and suppresses Phytophthora, and these methods are also impor-
tant components of integrated management programs (3,17).
Fungicides. Chemicals are widely recommended for Phytoph-
thora control, but their effectiveness is variable, particularly dur-
ing high-disease pressure in the wet season. The implementation
of recommendations is typically yield- and price-sensitive. Pro-
tectant sprays of copper-based fungicides, together with the sys-
temic fungicide metalaxyl, at 3- or 4-weekly intervals are fre-
quently recommended, but rarely cost-effective (12). Annual trunk
injections of the inexpensive inorganic salt potassium phospho-
nate are very effective against P. palmivora, particularly in reduc-
ing cankers, in very wet areas of Papua New Guinea (PNG) (12),
and in Ghana against both P. palmivora and P. megakarya (23).
Canker control can also be achieved by scraping surface bark to
expose the canker, then painting the affected area with a copper
fungicide.
Integrated management. Disease management strategies should
focus on eliminating sources of primary inoculum, in preventing
the movement of inoculum from the soil to the canopy, and in
reducing the production of secondary inoculum. Also, unlike
P. palmivora, the growth of P. megakarya is inhibited by light.
Shade and canopy management practices that increase light and
airflow within the canopy, such as appropriate spacing, pruning,
and weed control, are also likely to increase flowering and pod
development. Frequent and complete harvesting, sanitation, and
appropriate disposal of pod mummies, infected pods, and pod
husks will reduce the levels of inoculum and flying beetle vectors.
Piles of pod husks provide breeding sites for insect vectors and
discarded husks should be buried, preferably with the addition of
supplements that promote microbial activity and rapid decompo-
sition, such as chicken manure (3). Sanitation should also include
removal of ant tents (soil tunnels built on the trunk surface by
ants) that spread inoculum into the canopy.
Leaf litter mulches and ground covers reduce disease by pre-
senting a barrier to rain splash and by promoting the microbial
decomposition of Phytophthora-infected debris (17).
Care is needed to fully integrate Phytophthora management
into overall farm management. Whereas cultural control has been
shown to be effective in areas of Ghana where P. palmivora is the
only cause of black pod, canopy management, weed control, and
frequent harvesting alone did not control P. megakarya in Camer-
oon (20). However, when combined with fungicide applications,
sanitation provides useful control of both Phytophthora species
(23). Integrated disease management practices offer the best
promise of effective control of Phytophthora spp.; however, these
strategies depend on a thorough understanding of the biology of
the pathogen, the cropping cycle of the host under local condi-
tions and the education and active participation of farmers.
In PNG farmers are presented with a series of integrated dis-
ease and pest management options that are demonstrated during
field days and training programs (Table 1). However, the choice
of an option is considered, decided and implemented by the
farmer. Early results indicate a high level of interest and adoption
of these options, with impressive increases in yield.
Fig. 3. Cacao stem canker caused by Phytophthora palmivora.
TABLE 1. Integrated disease and pest management options for smallholdersa
Input level
Activity
Predicted yield
(kg db/ha)
Low Current smallholder practice 1.1
Medium Cocoa and shade tree pruning 2.0
Weekly harvests and sanitation
Weed control
High Cocoa and shade tree pruning 2.5
Weekly harvests and sanitation
Weed control
Fertilizers and manures
Canker treatment
Maximum Cocoa and shade tree pruning 3.3
Weekly harvests and sanitation
Weed control
Fertilizers and manures
Canker treatment
Insect vector control
aPredicted yields are based on results over 12 months on a farmer trial in Eas
t
New Britain Province (Papua New Guinea Cocoa Coconut Institute, 2007).
Vol. 97, No. 12, 2007 1653
CONCLUSIONS
Integrated disease management options should be developed
and promoted for smallholders in each region. P. megakarya
poses a significant threat to cocoa-growing regions outside West
Africa, and a concerted integrated global breeding program is in
progress to identify potential sources of resistance and other op-
tions for management.
The complex issues of Phytophthora, soil health and sustain-
ability of production need to be addressed in future research.
Healthy soils are characterized by high organic matter and plant
nutrient contents, abundant and diverse microbial activity, good
drainage and physical structure, and low levels of pathogen inocu-
lum. Understanding how to achieve and maintain healthy soils on
cocoa farms is fundamental to sustaining higher yields and lower
levels of disease, while minimizing environmental damage.
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