Technical paper
Distribution and management of Phaeoramularia leaf and fruit
spot disease of citrus in Ethiopia
Mohammed YESUF
Ethiopian Institute of
Agricultural Research,
PO Box 436, Nazareth,
Ethiopia
mohanarc@yahoo.com
Distribution and management of Phaeoramularia leaf and fruit spot disease
of citrus in Ethiopia.
Abstract –– Introduction. Citrus is the most important fruit crop widely grown by small-scale
and commercial farms in Ethiopia. However, productivity of citrus in many parts of the country
is threatened by Phaeoramularia leaf and fruit spot disease caused by Phaeoramularia angolensis.
Surveys and field experiments were conducted to map the geographical distribution, and to study
the efficacy of different fungicides for the control of this disease. Materials and methods. Surveys
were conducted in the major citrus-growing areas (south, south-west and north-west) of Ethiopia.
Random sampling techniques were used for sample collection. The efficacy of different fungicides
against P. angolensis was studied under a hot-spot area, based on disease incidence and severity,
and marketable fruit yield. Results and discussion. Phaeoramularia leaf and fruit spot disease
of citrus has been widespread throughout the south, south-west, and north-west of Ethiopia, causing complete crop failure. This disease was more severe in smallholder farmers' fields as compared
with the commercial orchards. The severity of P. angolensis was varied between different citrus
species and areas with different agro-ecologies. The south and south-west part of the country, characterized by high and frequent rainfall with high humidity, were severely affected by the disease.
Field application of Benlate, Score and Cuproxat significantly reduced the incidence and severity
of the disease and, thereby, increased marketable fruit yield. Conclusion. Phaeoramularia leaf
and fruit spot disease of citrus has become widespread in many parts of Ethiopia within a short
period. Further investigation on P. angolensis biology and detailed epidemiological studies are
mandatory to develop a model, and, thereby, to facilitate forecasting systems for effective and sustainable management of leaf and fruit spot disease of citrus in Ethiopia.
Ethiopia / Citrus / plant diseases / blotches / Phaeoramularia angolensis /
geographical distribution / disease control
Distribution et contrôle de la cercosporiose des agrumes en Éthiopie.
* Correspondence and reprints
Fruits, 2007, vol. 62, p. 99–106
© 2007 Cirad/EDP Sciences
All rights reserved
DOI: 10.1051/fruits:2007003
www.edpsciences.org/fruits
RESUMEN ESPAÑOL, p. 106
Résumé –– Introduction. En Éthiopie, la culture des agrumes est la production fruitière la plus
développée en petites exploitations comme en vergers commerciaux. Cependant, dans la majeure
partie du pays la productivité des arbres est menacée par la cercosporiose, maladie affectant les
feuilles et fruits des agrumes, et provoquée par Phaeoramularia angolensis. Des prospections et
une expérimentation en champ ont été menées afin de définir la répartition géographique de la
maladie, et d’étudier l'efficacité de divers fongicides utilisés pour son contrôle. Matériel et
méthodes. Des prospections ont été conduites dans les principales régions productrices (sud, sudouest et nord-ouest) d’agrumes en Éthiopie. Des techniques d’échantillonnage randomisé ont été
employées pour la collecte d’échantillons. L'efficacité de différents fongicides utilisés contre
P. angolensis a été étudiée dans un secteur de forte infestation, en se basant sur l'incidence et la
sévérité de la maladie, ainsi que sur le rendement en fruits commercialisables. Résultats et
discussion. La cercosporiose des agrumes s’est révélée répandue dans tout le sud, le sud-ouest
et le nord-ouest de l'Éthiopie y causant la perte décisive des récoltes. Cette maladie est apparue
plus grave dans les petites exploitations que dans les vergers commerciaux. La sévérité des attaques
dues à P. angolensis a varié selon les différentes espèces d’agrumes étudiées et l’agroécologie des
régions de production. Les régions du sud et du sud-ouest du pays, caractérisées par de fortes et
fréquentes précipitations et un taux d’humidité élevé, ont été sévèrement affectées par la maladie.
L’application en champ de Benlate, Score et Cuproxat a sensiblement réduit l'incidence et la
sévérité de la maladie et a accru le rendement en fruits commercialisables. Conclusion. La
cercosporiose des agrumes s’est répandue dans de nombreuses régions d’Éthiopie en peu de
temps. Davantage de recherche sur la biologie de P. angolensis et des études épidémiologiques
détaillées seront nécessaires pour développer un modèle, et, de ce fait, faciliter un système
d’avertissement pour une gestion efficace et durable de la cercosporiose des agrumes en Éthiopie.
Éthiopie / Citrus / maladie des plantes / cercosporiose / Phaeoramularia
angolensis / distribution géographique / contrôle de maladies
Fruits, vol. 62 (2)
99
Article published by EDP Sciences and available at http://www.edpsciences.org/fruits or http://dx.doi.org/10.1051/fruits:2007003
M. Yesuf
Figure 1.
Characteristic symptoms of
Phaeoramularia leaf and fruit
spot disease on sweet orange
(Citrus sinensis): (a) infected
leaves, (b) infected fruits,
(c) conidia of Phaeoramularia
angolensis.
1. Introduction
With a coverage estimated to be more than
5300 ha [1, 2], citrus is the most important
fruit crop widely grown in Ethiopia. However, in many parts of the country, citrus
productivity is threatened by a disease
called Phaeoramularia leaf and fruit spot
(figure 1). This disease, caused by a fungus,
Phaeoramularia angolensis (Covalho &
Mendes) Kirk, was first reported in Angola
and Mozambique in 1952. Within a short
period, the disease spread northwards to the
south of the Sahara [3–5]. Later it spread to
the eastern part of Africa: Uganda [6], Kenya
[5] and Ethiopia [7]. The disease has also
been reported in Yemen [6]. Leaf and fruit
spot disease of citrus is transmitted by airborne conidia or infected planting materials
100
Fruits, vol. 62 (2)
[8, 9]. Currently, the disease is widespread
and is becoming a major threat to citrus
plantation in 20 African countries including
Ethiopia [6, 10]. Leaf and fruit spot disease
of citrus has not yet been reported in the rest
of the world, except Yemen.
In Ethiopia, the characteristic symptoms
of leaf and fruit spot disease of citrus were
first observed in 1988 around the Aletawondo and Dale areas, near the border with
Kenya [11]. Later, in 1990, similar disease
symptoms were also apparent around
Bebeka and the south-west part of Ethiopia
[12]. The causal agent of the disease was
positively identified for the first time in Ethiopia to be Phaeoramularia angolensis [7].
The disease can cause a yield loss of (50 to
100)% in areas with high rainfall and humidity during the active growth stages of the
crop [13–15]. Currently, citrus plantations in
the south and south-west of Ethiopia are
seriously affected by this disease. Consequently, the supply of citrus fruits in these
areas has been insufficient for the last ten
years. Several small-scale citrus growers
have abandoned their trees due to severe
infection of citrus by the disease. The policy
of the Ethiopian government is presently to
promote fruit production, particularly citrus,
mainly to improve the nutritional standard
of the people and to obtain a source of
income for resource-poor farmers. However, leaf and fruit spot disease is becoming
the major limiting factor of the citrus industry. The national distribution, biology and
factors of disease epidemics of this pathogen have not yet been exhaustively investigated. Despite the devastating nature of the
disease, research efforts on disease distribution and management options to tackle this
disease are negligible.
Therefore, our research was initiated to
study the geographical distribution of the
disease and efficacy of fungicides for its
management in Ethiopia.
2. Materials and methods
2.1. Disease survey and
identification
Surveys were conducted in the major citrusgrowing areas of Ethiopia during the 2001
Phaeoramularia disease of citrus in Ethiopia
and 2002 crop seasons. Samples of infected
leaves and fruits were collected randomly
from all citrus species (sweet orange, mandarin, lemon, lime and grapefruit) present
in the 24 citrus orchards surveyed. From
each of these citrus orchards, 10 trees were
randomly selected towards the diagonal of
the field. Leaf samples were taken from different parts of the canopy (lower, middle
and upper) and, to assess the incidence and
severity of P. angolensis, 25 fruits were sampled from each tree. Samples were kept at
5 °C in a refrigerator. To avoid secondary
invaders, both leaf and fruit samples were
surface-sterilized using 1% sodium hypochlorite (NaOCl). Isolation was done by placing
pieces of tissue on Petri dishes with a
freshly-prepared potato dextrose agar
medium (PDA). The Petri dishes were then
kept for 7 d in an incubator under a temperature of (22 ± 1) °C, and then fungal
growth was examined under a binocular
and compound microscope. Single spore
isolation was carried out to obtain pure culture of P. angolensis.
2.2. Susceptibility of citrus species
to P. angolensis
Evaluation of different Citrus species
(C. aurantifolia, C. limon, C. paradisi,
C. reticulata and C. sinensis) was done for
their relative susceptibility to leaf and fruit
spot disease of citrus in a hot-spot area. Disease assessment was superimposed on the
already established citrus trees. From each
species, five trees and fifty fruits per tree
were randomly selected. Leaves were sampled from different canopy parts (lower,
middle and upper) and directions. Assessment of percent severity (percent of leaf and
fruit area covered by lesions) and number
of lesions on leaves and fruits was recorded
at different growth stages.
2.3. Fungicide screening
Various fungicides of different groups [Benlate® (benomyl, Du Pont de Nemours,
France, S.A.S.), different formulations of
Kocide® (copper oxychlorid, Du Pont de
Nemours, France, S.A.S.), Score® (difenoconazole, Syngenta Agro S.A.), Cuproxat®
(complex composition, Agrolinz, France),
and Cuprofix® (sulfate copper, Cerexagri]
were tested at Ghibe citrus orchard which
is a hot-spot area for leaf and fruit spot disease of citrus in Ethiopia. The experiment
was conducted for three consecutive years
(2000, 2001 and 2002), during the main crop
season, on sweet orange (Citrus sinensis
cv. Valencia) using a randomized complete
block design with four replications. Fungicides were applied, based on manufacturers' recommendations, every 2 weeks, using
a motorized knapsack sprayer. Each treatment was replicated four times by considering a single tree as a replicate.
Disease incidence on the foliage was estimated by counting total and infected leaves
of eight shoots randomly selected from four
directions of a tree. Disease incidence on
mature fruits was assessed using 50 randomly selected fruits from each tree after
harvest. Severity on leaves and fruits was
estimated based on percent area covered by
lesions of the disease.
2.4. Data analysis
Data were analyzed using the analysis of
variance (ANOVA) procedure. Mean separation tests were performed using Student’s
Newman Keuls test using SAS version 8.0.
3. Results and discussion
3.1. Disease surveys
The survey data indicated that Phaeoramularia leaf and fruit spot disease of citrus was
widely distributed throughout citrus-growing areas of the south, south-west and northwest parts of Ethiopia (figure 2). Eshetu [7]
reported in 1999 that this disease was distributed in the south and south-west of the
country. However, we noted that it has also
been widely distributed to the major citrusgrowing areas of the north-west part of Ethiopia. The incidence and severity of the disease varied across the agro-ecology of the
areas. Phaeoramularia leaf and fruit spot
disease of citrus was found to cause complete crop loss, especially on small-scale
peasant holdings. The south and south-west
Fruits, vol. 62 (2)
101
M. Yesuf
totrichum gloeosporioides, root rot (Phythophtora sp.), leaf spot (Alternaria sp.) and
fruit rot (Penicillium sp.) were found to be
important pathogens associated with citrus
in the surveyed areas, causing both preharvest and postharvest infection.
The observation that the severity of leaf
and fruit spot disease of citrus was more pronounced in smallholder farmers’ orchards as
compared with the commercial orchards
might be due to the fact that smallholder
farmers do not have technical know-how
and access to disease management practices. For instance, some commercial citrus
farms practiced sanitation measures and
were able to reduce pathogen buildup for
the coming crop season.
3.2. Susceptibility of citrus species
to P. angolensis
Figure 2.
Geographical distribution of
Phaeoramularia leaf and fruit
spot disease of citrus in
Ethiopia.
parts of Ethiopia (Ghibe, Jimma, Metu,
Wolisso and Wolkite) were found to be the
most affected as compared with the northwest regions (table I). Apart from
P. angolensis, anthracnose caused by Colle-
Evaluation of different citrus species in a
hot-spot area for relative susceptibility of
P. angolensis based on incidence and severity assessment indicated that grapefruit (Citrus paradisi) was the most susceptible citrus
species, followed by sweet orange (C. sinensis), mandarin (C. reticulata) and lemon
(C. limon), with lime (C. aurantifolia) being
the least susceptible (table II). More lesions
Table I.
Incidence and severity of Phaeoramularia leaf and fruit spot disease of citrus
assessed by surveys in different citrus-growing regions of Ethiopia.
Locations
102
Incidence1 %
Severity2 %
Leaves
Fruits
Leaves
Fruits
Aletawondo
89.6
88.4
78.4
82.4
Areka
85.5
83.8
76.2
78.5
Chagni
84.8
82.8
68.9
76.2
Fnoteselam
82.6
78.6
72.6
78.4
Ghibe
92.2
88.5
81.8
86.0
Gonder
64.5
78.6
52.4
65.6
Jimma
96.6
90.2
83.5
90.4
Metu
95.4
89.4
84.0
89.8
Wolkite
98.6
94.2
84.0
88.6
Wolliso
96.4
90.4
80.6
84.2
1
Incidence % = percent of leaves and fruits affected from the total per tree.
2
Severity % = leaf and fruit surface area covered by lesions (%).
Fruits, vol. 62 (2)
Phaeoramularia disease of citrus in Ethiopia
were counted during the wet and humid
seasons than during the dry seasons. The
number of lesions on both leaves and fruits
was higher around the lower tree canopy
than in the middle and upper canopy of
trees. This could be substantiated mainly
due to high moisture and humidity around
the lower tree canopy. Extended and high
rainfall during November and December
created favorable conditions for infection of
leaves and fruits in the Ghibe orchard. At the
early fruit-setting stage of the crop, the
severity of P. angolensis was more intense
on leaves than on young fruits. However, at
the later crop stages, the severity of the disease increased on fruits (figure 3).
3.3. Fungicide screening
Lower disease incidence and severity was
recorded from trees treated with Benlate,
Score and Cuproxat. Higher marketable fruit
yield was also obtained from trees treated
with Benlate, followed by Score and
Cuproxat (tables III, IV). Field application of
chlorothalonil was reported as effective
against leaf and fruit spot disease of citrus
in Ethiopia [7]. Application of Benlate by
alternating with copper compounds has also
been found effective to control P. angolensis
in Kenya [16].
Table II.
Relative susceptibility of different Citrus species, based on incidence
and severity assessment, to Phaeoramularia leaf and fruit spot
disease in a Ghibe citrus orchard (Ethiopia).
Citrus species
Incidence1 %
Severity2 %
C. aurantifolia
40
28
C. limon
56
33
C. paradisi
90
81
C. sinensis
75
52
C. reticulata
68
42
1
Incidence % = percent of leaves and fruits affected from the total per tree.
2
Severity % = leaf and fruit surface area covered by lesions (%).
incidence and severity of the citrus leaf and
fruit spot disease at Ghibe. Benlate and copper fungicides have been reported to be
effective against P. angolensis [16]. Field
application of chlorothalonil, copper hydroxide, flusilazole and propinebe provided good
control of the pathogen in East Africa [17].
Fungicide application should be done by
alternating from different chemical groups,
thereby avoiding development of resistance
by the target pathogen population. Since
Benlate is a systemic and expensive fungicide, it could be used by alternating with
Figure 3.
Severity of Phaeoramularia leaf
and fruit spot disease on sweet
orange cv. Valencia based on
area covered by lesions on
leaves and fruits at different
growing periods in Ghibe
(Ethiopia).
100
4. Conclusion
Leaf
Fruit
Application of Benlate, Score and Cuproxat
every 2 weeks significantly reduced the
80
Disease severity (%)
Phaeoramularia leaf and fruit spot disease
of citrus has been a recent introduction into
Ethiopia, and it was a problem in the south
and south-west part of the country [7]. However, in a very short time, this disease was
widespread in many citrus-growing areas of
the country including the south, south-west
and north-west parts of Ethiopia. The disease causes heavy loss to the citrus industry
in these areas. The most devastating effect
of the disease on all citrus species surveyed
is premature defoliation of young leaves and
fruit drop, and sunken lesions on the fruit
surface, which seriously affect their market
value. Infected fruits became extremely
hard, juiceless and unattractive (figure 1).
60
40
20
0
July
Aug.
Sept.
Oct.
Nov.
Dec.
Jan.
Months of the crop season
Fruits, vol. 62 (2)
103
Feb.
Mar.
Apr.
M. Yesuf
Table III.
Effect of fungicide spray on the incidence of Phaeoramularia leaf and fruit spot disease of citrus and marketable
fruit yield of sweet orange cv. Valencia in Ghibe (Ethiopia).
Fungicide
Active
substances
Control
2000/2001
2001/2002
Incidence on Incidence on Incidence on Incidence on
leaves
fruits
leaves
fruits
(%)
(%)
(%)
(%)
Marketable fruit
yield per tree
(kg)
–
58.7 a
67.3 a
58.0 a
69.3 a
75.6 c
Benomyl
31.0 f
38.0 d
31.3 f
40.7 de
130.7 a
Copper oxychloride
50% WP
44.3 bc
58.4 b
48.3 bc
58.0 b
79.3 bc
Cuprofix 78% WP
Copper sulfate
+ mancozeb
48.7 b
60.3 b
51.3 b
58.0 b
84.6 bc
Cuproxat 54% SC
Complex composition
with copper sulfate
40.7 cd
48.7 c
39.0 d
45.7 cd
91.8 b
Benlate 50% WP
–
Kocide 101 77% WP
Cupric hydroxide
47.3 b
52.0 c
44.7 c
49.3 c
84.0 bc
Kocide 2000 53.8% WP
Copper hydroxide
36.3 de
48.7 c
37.3 de
48.3 c
82.3 bc
Diphenoconazol
32.0 ef
41.7 d
34.0 ef
39.3 e
124.7 a
Mean
42.4
51.9
43.0
51.1
94.1
Coefficient of variation (%)
12.6
10.8
14.5
11.4
9.6
Score 25% EC
Means followed by the same letter(s) in a column are not significantly different using Student’s Newman Keuls test at (P = 0.05).
Table IV.
Effect of fungicide spray on the severity of Phaeoramularia leaf and fruit spot disease of citrus and marketable
fruit yield of sweet orange cv. Valencia in Ghibe (Ethiopia).
Fungicides
Active
substances
Control
2000 / 2001
Severity on
leaves
(%)
Severity on
fruits
(%)
2001 / 2002
Marketable fruit
yield/tree
(kg)
Severity on
leaves
(%)
Severity on
fruits
(%)
–
21.4 a
31.7 a
68.4 c
21.7 a
29.9 a
Benomyl
9.1 c
13.3 d
126.8 a
11.8 de
10.1 d
Copper oxychloride
50% WP
16.3 b
25.1 b
75.0 bc
17.8 abc
19.0 ab
Cuprofix 78% WP
Copper sulfate
+ mancozeb
14.7 b
21.6 bc
83.8 bc
18.5 ab
16.3 abc
Cuproxat 54% SC
Complex composition
with copper sulfate
12.4 b
19.6 c
88.4 b
14.4 cd
14.4 c
Kocide 101 77% WP
Cupric hydroxide
16.3 b
21.2 bc
76.2 bc
16.3 bc
16.6 abc
Kocide 2000 53.8% WP
Copper hydroxide
14.2 b
18.8 c
74.5 bc
14.3 cd
15.2 bc
Diphenoconazol
Benlate 50% WP
–
Score 25% EC
8.9 c
12.7 d
118.6 a
9.9 e
10.6 d
Mean
14.2
20.5
89.0
15.6
15.3
Coefficient of variation (%)
16.1
12.4
12.2
13.9
13.8
Means followed by the same letter(s) in a column are not significantly different using Student’s Newman Keuls test (P = 0.05).
104
Fruits, vol. 62 (2)
Phaeoramularia disease of citrus in Ethiopia
copper fungicides, thereby avoiding pathogen resistance and reducing fungicide application costs. Production of citrus should
concentrate on the lower altitude and semiarid areas of Ethiopia with low rainfall,
which are not conducive to the development of leaf and fruit spot disease of citrus.
Sources of resistance of citrus species
against P. angolensis and detailed epidemiological studies should receive future
research attention.
Acknowledgements
The author would like to thank the Horticulture Development Enterprise (HDE) for
providing the experimental citrus trees of
their farm in Ghibe. The management of
Melkassa Agricultural Research Center is
also acknowledged for logistical support.
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105
M. Yesuf
Distribución y control de la cercosporosis de los cítricos en Etiopía.
Resumen –– Introducción. En Etiopía, el cultivo de los cítricos es la producción de frutos
más desarrollada en pequeñas explotaciones como en los huertos comerciales. No obstante,
en la mayor parte del país, la productividad de los árboles está amenazada por la cercosporosis, enfermedad que afecta las hojas y los frutos de los cítricos y provocada por Phaeoramularia angolensis. Se llevaron a cabo prospecciones así como un experimento en campo, con
el fin de definir el reparto geográfico de la enfermedad y de estudiar la eficacia de diversos
fungicidas usados para su control. Material y métodos. Se llevaron a cabo prospecciones en
las principales regiones productoras (sur, sudoeste y noroeste) de cítricos en Etiopía. Se
emplearon técnicas de muestreo aleatorio para la colecta de muestras. Se estudió la eficacia
de los diferentes fungicidas empleados contra P. angolensis en un sector con plagas pronunciadas, basándose en la incidencia y en la gravedad de la enfermedad, así como en el rendimiento en frutos comercializables. Resultados y discusión. La cercosporosis de los cítricos
resultó extendida por todo el sur, suroeste y en el nordeste de Etiopía, causando de este
modo la pérdida importante de las cosechas. Esta enfermedad se mostró más severa en las
pequeñas explotaciones que en los huertos comerciales. La gravedad de los ataques causados
por P. angolensis varió de acuerdo con las diferentes especies de cítricos estudiados y con la
ecología agraria de las regiones de producción. Las regiones del sur y del suroeste del país,
caracterizados por precipitaciones fuertes y frecuentes y por un alto índice de humedad, fueron gravemente afectadas por la enfermedad. La aplicación en campo de Benlate, Score y
Cuproxat redujo sensiblemente la incidencia y la gravedad de la enfermedad y aumentó el
rendimiento de frutos comercializables. Conclusión. La cercosporosis de los cítricos se
extendió en numerosas regiones de Etiopía en poco tiempo. Serán necesarias más investigaciones de la biología de P. angolensis, así como estudios epidemiológicos detallados con el
fin de desarrollar un modelo; y, de este modo, facilitar un sistema de advertencia para una
gestión eficaz y duradera de la cercosporosis de los cítricos en Etiopía.
Etíopia / Citrus / enfermedades de las plantas / cercosporiose / Phaeoramularia
angolensis / distribución geográfica / control de enfermedades
106
Fruits, vol. 62 (2)
Mohammed Yesuf