Coffee Wilt Disease (Gibberella xylarioides Heim and Saccas) in Forest Coffee Systems of Southwest and Southeast Ethiopia
Coffee diseases are presumed to be less important in the forest coffee as compared to the garden and plantation systems of coffee production in Ethiopia. In this article, the results of a study conducted on the occurrence and incidence of Coffee Wilt Disease (CWD) and the major factors influencing the disease in four major forests coffee sites in southwest and southeast Ethiopia are discussed. In each forest coffee site, coffee wilt syndrome was assessed in three systematically selected sample plots during dry and wet seasons of 2008 and 2009. Concurrently, three to four samples of infected coffee trees were randomly collected from each plot and the causal pathogen was isolated and identified in the laboratory. The result indicted that CWD was prevalent in the four forest coffee sites, with mean incidence of 27.1 and 29.2% in Harenna during 2008 and 2009 wet seasons, respectively, followed by Berhane-Kontir with mean incidences of 22.1 (2008) and 27.7% (2009). Whereas, Bonga and Yayu forest coffees had comparatively low wilt severity (<10%). The wood samples of most of the infected coffee trees (90.6%) yielded Gibberella xylarioides in the laboratory proving that this pathogen is the main cause of coffee tree death in the forest. The difference in incidence of CWD across the four sites and among fields was strongly associated with human factors and variations in coffee populations. The forest coffee trees in Harenna and Berhane-Kontir (high CWD) are almost transformed to semiforest type by sub-planting coffee seedlings after thinning the dense vegetation cover. These activities are known to create wound to the host and disseminate the fungus spores from tree to tree and from one field to the other. The two independent seedling inoculation tests in the greenhouse evidenced that there were significant variations among coffee accessions in reactions to CWD though most accessions were susceptible. The study showed that CWD is one of the potential biotic factors threatening the genetic diversity of Arabica coffee in most forest coffee sites and thus the disease management practices should duly be considered in planning and implementing forest coffee conservation strategy.
November 24, 2011; Accepted: April 26, 2012;
Published: June 27, 2012
Arabica coffee (Coffea arabica L.) has its centre of origin in the highlands
of southwest and southeast Ethiopia where wild coffee trees still
grow naturally in the understory of the fragmented montane rainforests. Among
the four coffee production systems known in the country, forest and semiforest
coffees are believed to possesses the largest coffee genetic resources (gene
pool) followed by the landraces with enormous potential to improve
the crop (Sylvain, 1958; Meyer,
1965; Van der Graaff, 1981; Mesfin,
1991; Paulos and Demel, 2000; Gole
et al., 2002; Tesfaye, 2006; Tadesse
et al., 2008).
Nevertheless, settlement and agricultural land-use pressure have been persistently
reducing the remaining forest fragments inhabiting wild coffee populations and
other invaluable biodiversity. Poverty and conflicting property rights make
farmers convert forests into agricultural or pastoral land, thereby threatening
the entire biodiversity of the forests. Consequently, coffee genetic erosion
has gone far beyond the point of no return (Mesfin, 1991;
Paulos and Demel, 2000; Tadesse et
al., 2008). Apart from threats posed by biological and ecological processes,
the impact of insect pests and diseases on the forest coffee populations are
little understood except presumption from limited observations that they are
less important in the forests.
There are, however, many research findings documented on diseases and insect
pest situations in semiforest, garden and plantation coffee production systems,
which originates from the wild forests in Ethiopia (Van
der Graaff, 1981; Merdassa, 1986; Eshetu
et al., 2000; Girma et al., 2009a).
Coffee wilt is one of the three economically important diseases dramatically
limiting coffee production in the country. It is caused by a fungal pathogen
commonly known by its teleomorphic name Gibberella xylarioides Heim and
Saccas (Fusarium xylarioides Steyaert) that totally kills coffee plant
at any growth stage in all production systems. The disease is more prevalent
in plantation and garden coffee than semiforest coffee (Girma
et al., 2001; Girma et al., 2009a).
The disease incidence ranged from 3.6 to 15.5% in semiforest coffee of southwest
coffee-producing areas, while about 18.6 and 25.4% was estimated in some garden
coffee fields in the southern region (CAB International,
2003; Girma, 2004). In large-scale plantation, the
mean incidence varied from 45% at Gera to about 69% at Bebeka and it is more
serious in small-scale farmers coffee plantations with mean incidence
ranging from 21.7 to 77% (Girma et al., 2009a).
According to CAB International (2003), coffee production
(yield) at the farm level decreased by 37% and this led to a decline in income
of 67%. The national incidence and severity of CWD in Ethiopia were 27.9 and
5%, respectively, with estimated monetary loss of more than 3.8 million US$
annually (CAB International, 2003; Girma
et al., 2009a).
The occurrence of CWD in the forest coffee systems was first noted by Arega
(2006) with average tree death of 16.9%. This survey work was not, however,
accompanied by disease sample collection, isolation and identification of the
causal agents involved in the coffee tree death complexes including multitude
of biotic and abiotic factors. Thus, the incidence and distribution of coffee
wilt syndrome and its causal pathogen along with examining the important factors
influencing the disease progress thereby impacting the forest coffee genetic
resources in southwest and southeast Ethiopia is presented in this article.
MATERIALS AND METHODS
Descriptions of the study sites: The study was conducted in the field,
in the laboratory and in the greenhouse between the period 2008 and 2010. Coffee
wilt disease surveys were carried out in sample fields at four rainforest coffee
sites of Bonga, Berhane-Kontir and Yayu in the southwest and Harenna in the
southeast Ethiopia. The laboratory and greenhouse studies were undertaken in
Plant Pathology laboratory at Jimma Agricultural Research Center (JARC) situated
12 km away from Jimma town. Bonga forest coffee is found in Gimbo district of
the Kafa zone while Berhane-Kontir forest coffee is located in Sheko district
of Bench Maji zone in Southern Nations Nationalities and Peoples Regional
state. Yayu forest coffee represents the major part of Geba-Dogi forest sites
delineated in Yayu district of Illubabor zone. Harenna forest coffee is the
major part of most eastern Afromontane rainforests that also constitutes the
largest subsection of the Bale Mountains National Park in southeastern Ethiopia
(Feyera, 2006). The detailed agroecological conditions
of the four forest coffee sites and that of Jimma are well illustrated by Kufa
and Burkhardt (2011a, b).
Disease assessment and sample collection: Three representative sample
fields (20x20 m area/field) were randomly selected for coffee wilt disease (CWD)
assessment and disease specimen collection in the four forest coffee sites.
The disease assessment was conducted by diagnosing wilting/dying coffee trees
for CWD, Armillaria root rot and other agents based on external and internal
symptoms of the respective diseases and signs of the causal pathogens such as
stromata and rhizomorph structures (Girma et al.,
2001; Girma, 2004; Girma et
al., 2009a). Finally the number of wilted/dead and healthy coffee trees
were counted and recorded according to the observed symptom categories.
The disease distribution pattern and foci development in the forests was thoroughly
studied in relation to topography, slope/gradient and above all the nature of
the forests (intact or disturbed) based on the degree of human interferences
measured by management activities such as thinning forest vegetation, weeding
and sub-planting coffee seedlings. At same time, three stem pieces (20 cm long)
were collected from three to four samples of infected coffee trees with wilting
or die-back symptoms in each field, and kept in perforated plastic bags labeled
with name of locality, sample number and collection date. The wood samples were
transported to JARC Plant Pathology laboratory and maintained at 4°C until
isolation (Girma and Mengistu, 2000; Girma,
2004). The disease survey was conducted twice, the first one was in January
2008 representing dry season soon after harvesting and the second was during
the raining season in August 2009.
Isolation and identification of causal pathogens in the laboratory:
The disease causal pathogen was isolated and identified according to the standard
laboratory procedures (Booth, 1971; Girma
and Mengistu, 2000; Girma, 2004; Rutherford
et al., 2009). Four to five wood pieces (1 cm) were excised using
scalpel after gently removing the bark from each of the samples and disinfected
in plastic petri dish with 10% Clorox (NaHCO3). The disinfected sections
were plated on potato sucrose agar (PSA) and incubated for 5 to 7 days. The
emerging colony out of the plated pieces were purified by hyphal tip method
and sub-cultured on PSA and then incubated for 10 to 14 days under 12 h light
and dark cycle. The cultural and morphological characteristics of the pure cultures
were used to identify Gibberella xylarioides and other Fusarium
spp. as described by Booth (1971), Girma
and Mengistu (2000) and Rutherford et al. (2009)
and in reference to the earlier Fusarium collections preserved in the laboratory
Seedling inoculation tests of coffee accessions collected in the forest
sites: There were two sets of seedling inoculation experiments conducted
in the greenhouse to determine the diversity of forest coffee populations in
reactions to the pathogen isolate following the recommended technique by Girma
et al. (2009b). In set I experiment, the inoculation test was performed
on 60 coffee accessions originated from three different fields (15 accessions/field)
representing the four forests coffee sites (Bonga, Berhane-Kontir, Yayu and
Harenna) and properly maintained at JARC for various research purposes. The
second set consisted of 20 coffee accessions randomly collected from fruit bearing
coffee trees in all forest sites except Berhane-Kontir in November 2008.
Seed preparation and raising coffee seedlings: Coffee seeds were prepared
from each accession separately following the routine practices that fully ripe
red cherries were picked, hand pulped and dried under lathouse shade. Seedlings
were raised by sowing the coffee seeds in sterilized and moistened sandy soil
in plastic pot with 5.8 L volume (20-25 seeds/pot and 3 pots/accession) after
removing the parchment and soaking overnight. Coffee cultivars with known ranges
of resistance to CWD (resistant, moderate and susceptible) were included as
checks in each set of the experiments (Girma et al.,
Inoculum multiplication and inoculation of coffee seedlings: Two Gibberella
xylarioides isolates namely Gx2 and Y-21 were deliberately
(known for pathogenicity) selected for inoculation tests in set I and set II
experiments, respectively. The former isolate represented large Fusarium collections
in plantation coffee while the latter was collected in Yayu forest coffee. At
cotyledon stage of the seedlings (2 month after sowing), inocula of the two
isolates were separately multiplied on sterile coffee twigs placed in test tubes.
After 14 days incubation, conidia were harvested by scratching and rinsing from
the branches with distilled sterile water and the concentration of spore suspension
was counted with haemocytometer and then adjusted to 2.0x106 conidia
mL-1 (Girma and Mengistu, 2000; Girma
et al., 2009b). The seedlings of each coffee accession were subsequently
inoculated with viable conidial suspension by stem nicking technique described
by Pieters and van der Graaff, (1980) and Girma
et al. (2009b). All the treated plants were then placed on experimental
benches and immediately covered with plastic sheet in a growth room with high
humidity and temperature of about 23°C to favour infection (Girma
et al., 2009b). After 10 days, the inoculated seedlings were transferred
into greenhouse and the treatments were arranged in Randomized Complete Block
Design (RCBD) with three replications (pots) having 20 inoculated seedlings
Data collection and statistical analysis: Based on the typical wilting
symptoms and death of the seedlings, the number of wilted/dead and healthy seedlings
were counted and recorded per pot every two weeks for six months starting a
month after inoculation. Isolation from samples of inoculated seedlings was
made when necessary. The percentages of dead seedlings were computed from the
cumulative number of dead seedlings (during the 6 months period) over the total
number of inoculated seedlings.
Similarly, the percentages of CWD infected coffee trees were calculated for
the disease assessment in the fields, while proportions of isolation was calculated
from the total number of collected and plated specimens from each forest coffee
site. The percentage data sets were transformed to angular values before statistical
analysis with SAS system for windows (9.2 version) (SAS,
2008). Treatment means are compared and separated based on LSD values when
F-test showed significance.
Distributions of coffee wilt disease in forest coffee systems: Coffee wilt disease was prevalent in forest coffee systems in the southwest and the southeast Ethiopia. The disease incidence varied from field to field and from one survey area to the other. During the dry season of 2008, the incidence ranged respectively from 0 to 15.4%, 7.3 to 37.6%, 0 to 22.3%, and 26.4 to 28.3% in Bonga, Berhane-Kontir, Yayu and Harenna (Fig. 1). During the wet season of 2009, the average disease incidence was 11.9, 29.2, 13.2 and 27.7% at the respective forest sites (Fig. 2).
Isolation and identification of the fungus from collected samples:
Gibberella xylarioides was the predominant pathogen isolates (90.6%) identified
from randomly collected samples of infected coffee trees in the four forest
coffee sites of Bonga, Berhane-Kontir and Yayu in southwest and Harenna in southeast
||Incidence of coffee wilt disease (CWD) in different fields
of four forest coffee sites of southwest and southeast Ethiopia in dry season,
||Incidence of coffee wilt disease (CWD) in different fields
of the forest coffee sites of southwest and southeast Ethiopia in wet season,
||Proportions (%) of Gibberella xylarioides isolates
and other unidentified spp. from wood samples of infected coffee trees collected
in southwest and southeast forest coffee sites of Ethiopia
The remaining 9.4% of the samples produced unidentified microorganisms including
other Fusarium spp. (Fig. 3).
||Reactions of forest coffee accessions to Gibberella xylarioides
Gx2 isolate in seedling inoculation test under greenhouse conditions
at Jimma Research Centre (set I experiment)
|1Susceptible, 2Moderately resistant
and 3Resistant Arabica coffee varieties to CWD in seedling tests
(Girma et al., 2009b) used as check, *Coffee
accessions coded as P111-P135, P211-P235, P311-P335, P411-P435 were respectively
collected from Harenna, Bonga, Berhane-Kontir and Yayu forest coffee sites.
Means with the same letter(s) are not significantly (p<0.05) different
from each other
Isolation and identification results demonstrated that the highest proportion of coffee tree deaths are largely caused by coffee wilt disease infected by Gibberella xylarioides proving that this disease is significantly threatening the forest coffee populations. There were, however, some died coffee trees caused by Armillaria root rot as the infected trees easily toppled down and the dark rhizomorphs of Armillaria mellea were detected in the roots. Also few coffee trees exhibited neither symptom of infection nor signs of the casual agents rather seem physiological dieback.
Seedling inoculation tests of forest coffee accessions: There were significant
(p<0.01) differences among the tested coffee accessions collected in the
forest sites in seedling inoculation experiments.
||Reactions of randomly collected forest coffee accessions to
Gibberella xylarioides Y-21 isolate in seedling inoculation
test under greenhouse conditions at Jimma Research Centre (set II experiment)
|1Susceptible and 2Resistant (Girma
et al. 2009b), *Coffee accessions coded as HA1-HA8, BO1-BO4 and
YA1-YA2 were respectively collected from Harenna, Bonga and Yayu forest
coffee sites ++ and 0.0 indicates no external symptom was observed on these
accessions and thus no incubation period was detected, respectively. Means
with the same letter(s) are not significantly (p<0.01) different from
In set I experiment that consisted of 60 coffee accessions originated from
the forest, seedlings of almost all of the Harenna accessions (P111-P135) showed
the lowest infection by Gibberella xylarioides isolate Gx2
with less than 2% seedlings death that was not significantly (p<0.05) different
from the two resistant checks Catimor J-19 and Catimor J-21
(Table 1). Among the tested 15 coffee accessions P111, P114,
P125, P131, P132 and P134 have remarkably exhibited no wilting symptom. On the
contrary, most coffee accessions obtained from Bonga (P211-P235), Berhane-Kontir
(P311-P335) and Yayu (P411-P435) showed significantly (p<0.05) higher seedling
deaths of about 80 percent as compared to the standard susceptible control SN-5
In set II experiment, coffee accessions randomly collected in the fields of three forest areas and inoculated with the isolate from Yayu forest Y-21 showed highly significant (p<0.01) differences both in percent seedling death (wilt) and incubation period. Similar to the result of set I experiment, half of the Harenna coffee accessions HA1, HA2, HA6 and HA8 had very low seedling deaths ranging from 0 to 10 percent with longer incubation periods. While significantly (p<0.01) higher seedling death of 90 percent was recorded on coffee accessions from Bonga (BO1, BO2), Yayu (YA1, YA2) and Harenna (HA3, HA4) than the susceptible check SN-5 (Table 2). The results of both sets of inoculation experiments implied that most coffee trees in the forest except those from Harenna site are highly susceptible to coffee wilt pathogen infection.
Coffee wilt is a systemic vascular disease caused by a fungal pathogen commonly
referred by its teleomorphic nomenclature Gibberella xylarioides Heim
and Saccus. The disease attacks all commercial Coffea spp. including
Coffea arabica and Coffea canephora at any growth stage. Although,
it is currently restricted to coffee producing countries in East and Central
Africa, the disease can be a potential threat to the world coffee production
(Rutherford, 2006; Girma et al.,
2009b). It is one of the major factors constraining coffee production with
rapid prevalence in plantation, garden and semiforest coffee production systems
in Ethiopia (Girma et al., 2009a).
In addition, the present study evidenced that coffee wilt disease is causing
significant losses to coffee trees in the forest coffee systems inhabiting invaluable
gene pools of Coffea arabica. The highest mean incidence of 27.1% was
recorded at Harenna forest coffee in the southeast followed by Berhane-Kontir
with 24.9% in southwest Ethiopia during the dry season of 2008. In the following
season, it was more pronounced at Berhane-Kontir (29.2%) albeit similar trend
was observed in Harenna forest. Some three years back, the mean percent coffee
tree death estimated by Arega (2006) was about 2.4% at
Berhane-Kontir while the highest was 17% at Yayu coffee areas. The overall comparison
in CWD progress over the years implicates that the disease pressure is rapidly
increasing in the forest coffee systems across all sites, although, slight increment
of about two to five percent was recorded during the subsequent wet season.
A remarkable increase in CWD severity of about 11.5% was estimated over a 6-month
period in nine districts of Gedeo and Sidama zones of Ethiopia (CAB
International, 2003; Girma et al., 2009a)
which are largely characterized by producing world renowned fine Arabica coffee
(Yirgacheffe and Sidamo speciality) in the garden coffee
The spatial distribution of coffee wilt epidemics was found to decrease from
the more disturbed peripheral parts towards the centers of the intact (undisturbed)
forest coffee systems except in the fields at Harenna and Berhane-Kontir sites.
The disease occurrence dropped from 15.4 to 0.0 and from 19.6 to 0.0% across
the fields (from field 1 to field 3) at Bonga and Yayu forests, respectively
(Fig. 1). These differences in progression over seasons (years)
and spaces could be ascribed primarily to human factors (degree of human exploitation
of the forest coffee) in addition to the variations in coffee populations and
may be to the fungus strains. The coffee trees at Berhane-Kontir and Harenna
forests, where CWD incidences were high and epidemics were fairly uniform throughout
the fields, are almost transformed to semiforest type as farmers have been intensively
exploiting the so called wild coffee. It was observed that, in order
to harvest good yield and maximize income, the dense tree stands of upper forest
strata have been thinned out, bushes and shrubs were removed and then transplanted
with self-raised or naturally regenerated coffee seedlings from year to year.
Feyera (2006) evidenced that the difference between managed
(semiforest) and undisturbed forest was minimal as the number of plant species
declined by 50% and the only dominant stand was coffee in Yayu, Harenna and
Berhane-Kontir areas. The author found that grazing animals, frequent weeding
(2 to 4 times per year) and clearing all the herbaceous vegetation were the
common activities from year to year (Feyera, 2006). These
activities are known to facilitate dissemination of the fungus ascospores and
conidia within and across the fields and create wounds to the host thereby favoring
coffee wilt development and prevalence (Girma et al.,
2001; Girma et al., 2009a; Phiri
et al., 2009; Rutherford et al., 2009).
On the other hand, besides the non human impacts in the undisturbed forests,
the low incidence might be due to the suppression of the fungal pathogen by
the natural communities of bacteria and fungal species. Mekete
et al. (2008) recorded a large number of endophytic bacteria (201)
and fungi (128) including non-pathogenic Fusarium and Trichoderma
spp. in forest coffee agroecologies of Ethiopia. Besides, the antagonistic
potential of 21 bacterial isolates that significantly inhibited the mycelial
spread of Gibberella xylarioides in vitro was reported by Muleta
et al. (2007).
The results of greenhouse inoculation experiments proved that there is important
diversity in coffee populations (within and among the forest sites) in reaction
to G. xylarioides infection. However, there is a tendency towards occurrence
of higher frequency of susceptibility reactions except in Harenna coffee populations
that consistently revealed higher level of resistance in both sets of experiments,
even despite the fact that relatively more CWD incidence recorded in the fields.
Arega (2006) also reported similar findings that 50%
(five out of ten) of Harenna coffee collections showed less than 15% seedling
deaths, as opposed to coffee accessions collected in Bonga (16), Berhane-Kontir
(20) and Yayu (20) forest areas which showed more than 85% average infections.
The inconsistent response of Harenna coffee populations in the field and the
greenhouse conditions could perhaps be the difference in aggressiveness of the
pathogen isolates used in the seedling inoculation tests, as they were originated
from southwest Ethiopia. This in turn warrants studying host pathogen interactions
among coffee accessions and the pathogen strains representing forest coffee
systems, as variations in aggressiveness among the pathogen populations was
already reported by a number of workers (Adugna et al.,
2005; Girma et al., 2009b; Rutherford
et al., 2009).
In conclusion, the present assessment supported by detailed diagnosis coupled
with frequent isolation and identification of the causal pathogen Gibberella
xylarioides, coffee wilt disease is proved to be prevalent in the forest
coffee systems in southwest and southeast Ethiopia. The disease incidence, although
varying from field to field and from one forest coffee site to the other, has
been increasing spatially and temporally thereby becoming one of the major factors
threatening forest coffee genetic resources. It is decimating those coffee trees
that perhaps possessing resistances to other diseases, insect pests and nematodes;
with good yield and quality attributes like low caffeine content. Thus, the
forest coffee conservation strategies should take the disease into account and
apply the recommended principles and practices of CWD management (Girma
et al., 2009a; Negussie et al., 2009;
Phiri et al., 2009). Development of CWD resistant
Arabica coffee varieties through large-scale collection and screening against
the pathogen would be inevitable, although it seems that most coffee trees exhibit
susceptibility in the forest coffee populations.
Gibberella xylarioides is isolated and identified from infected coffee wood samples collected in the intact and undisturbed forest sites. This finding provides additional insight that the Arabica isolates of the pathogen is independently descended/evolved population on its hosts. However, this requires further survey and many more isolate collections (exploring in other intact coffee forests) with subsequent characterization and analysis of the population structure employing the recent molecular approaches hand-in-hand with host-pathogen interactions.
The authors would like to acknowledge the German Federal Ministry of Education
and Research (BMBF) for sponsoring this research work through Center for Development
Research (ZEF). We are indebt to Jimma University (JUCAVM) and JARC for providing
laboratory and greenhouse facilities. Dr. Tadesse W. Gole and his ECFF team
really deserve heart-felt thanks for their interest and consideration of Phytopathological
problems in the research project. Finally, a special appreciation to all Plant
Pathology staffs for their technical assistance in the field, laboratory and
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