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World Journal of Agricultural Sciences 17 (5): 418-429, 2021
ISSN 1817-3047
© IDOSI Publications, 2021
DOI: 10.5829/idosi.wjas.2021.418.429
Corresponding Author: Dereje Amare, Ethiopian Institute of Agricultural Research,
Holleta Agricultural Research Center, Addis Ababa, Ethiopia.
418
Coffee Leaf Rust Disease and Climate Change
Yitagesu Tadesse, Dereje Amare and Asela Kesho
Ethiopian Institute of Agricultural Research,
Holetta Agricultural Research Center, Addis Ababa, Ethiopia
Abstract: Coffee is the most important agricultural commodity and second most valuable commodity exported
by developing countries. Despite the largest share in production and economic contribution, C. arabicais
prone to several diseases among them coffee leaf rust (CLR) is the most destructive coffee disease in the world.
It causes losses of 1-2 billion USD annually and is one of the main limiting factors of Arabica coffee production
worldwide. Climate change threatens crop yields, both directly through changes in plant growth and production
and indirectly through impacts on crop diseases. It has been estimated that changes in climate have already
been reducing global agricultural production by 1-5% per decade over the last 30 years. CLR was not
problematic above 1000 m.a.s.l until the post-2011 epidemic, when CLR infestations of equal intensity were
observed from 400 to 1400 m.a.s.l due to climate change. The primary weather-related variables that affect CLR
include temperature, moisture and wind. As average minimum temperatures increase, the incidence and severity
of CLR epidemics also increases, more areas at higher elevations likely will become favorable to CLR. Moisture
plays a key role in the progress of CLR, affecting the germination, infection and spread of spores and the overall
health of the coffee plants. Understanding the climate and weather connections to CLR outbreaks may allow
farmers to prepare for and manage the disease more effectively and ultimately reduce crop losses. In future,
further research will be focused on discovering climate change adaptation strategies feasible for smallholder
producers for practically implement.
Key words: Coffee arabica Coffee Leaf Rust Hemileia vastatrix Climate change Temperature
INTRODUCTION Coffee leaf rust (CLR) is the most destructive coffee
Coffee is the most important agricultural commodity; production since the late 1800s [5]. CLR causes losses of
worth an estimated retail value 70 billion USD, crucial for 1-2 billion USD annually and is one of the main limiting
the economy of more than 70 countries. Coffee is the factors of Arabica coffee (Coffea arabica) production
second most valuable commodity exported by worldwide [5]. CLR was first recorded by an English
developing countries [1, 2]. There are more than 100 explorer in 1861 near Lake Vitoria (East Africa) on wild
coffee species but only two, Coffea arabica (Arabica) Coffea species. Soon after its first report, the disease
and Coffea canephora (Robusta), are commercially used wiped out coffee cultivation from Ceylon (Sri Lanka), with
for the production of coffee as a beverage. devastating social and economic consequences [6].
Despite the largest share in production and economic The pathogen affects living leaves and causes chlorotic
contribution, C. arabica is prone to several diseases lesions on the underside of the leaves. This reduces the
among which coffee berry disease (CBD), coffee wilt photosynthetic area and in severe attacks, defoliation of
disease (CWD) and coffee leaf rust (CLR) caused by leaves leading to die-back of branches with heavy losses
Colletotrichum kahawae Waller and Bridge, Gibberella for farmers. CLR damages coffee plants and decreases
xylarioides (Steyaert) Heim and Saccas and Hemileia yields, which in turn reduces labor, influences wages,
vastatrix Berk. and Br.,respectively, are the major fungal affects market prices and inhibits farmers’ ability to
diseases [3, 4]. manage their farms. The cumulative effects reduce farmer
disease in the world and has negatively impacted coffee
World J. Agric. Sci., 17 (5): 418-429, 2021
419
income, affecting livelihoods and food security and force convergence of several agronomic, climatic and economic
some to abandon their farms or switch to different crops factors [12, 20, 21]. Yield losses were up to 35%, with a
altogether [7]. direct impact on the income and livelihood of hundreds of
Nine major dominant resistance factors to H. thousands of farmers and laborers. The pathogen can
vastatrix have been so far inferred on the basis of the cause foliage loss up to 50% and berries up to 70% [22].
gene-for-gene concept. The resistance to leaf rust of Plant pathogens, including fungi, bacteria and
coffee plants therefore appears to be conditioned by at viruses are significant biotic limitations to production in
least nine resistance genes designated as SH1–SH9, either managed agricultural and forest systems. Temperature,
singly or in combination, while the corresponding relative humidity and precipitation are major factors
virulence have been indicated as V1–V9 [8]. This allows contributing to the incidence and severity of plant
coffee genotypes to be classified in resistant groups diseases. Many plant pathogens co-evolved with their
according to the physiological races of the rust pathogen hosts, developing optimal growth conditions in
[9]. Of the 9 resistance factors, SH1, SH2, SH4 and SH5 concurrence, so that outbreaks may occur under
have been found in C. arabica. The other genes, SH6, otherwise optimal agronomic conditions [23]. Plant
SH7, SH8 and SH9, have been introgressed from the pathogens can thrive in high moisture environments,
diploid species C. canephora, while SH3 probably which favor establishment, growth and infection of
originates from another diploid species, C. liberica. susceptible hosts. Moderate rain events can increase
In the second half of the 20th century, the disease in susceptible crops, as fungal spores are
identification and characterization of “Híbrido de Timor” splash-dispersed onto wet plant surfaces [24].
(HDT) populations provided the basis for a breeding The production of coffee declined by around 40%
program that enabled the release of rust-resistant cultivars due to a severe CLR outbreak that occurred across
in different coffee growing countries, including the Colombia and neighboring Latin American countries from
Americas [10, 11]. CLR epidemics have been particularly 2008 to 2013 [12]. Several hypotheses have been
damaging in Latin American and the Caribbean [12]. proposed to explain the recent CLR outbreak, including
In 2012–2013, CLR epidemics cost farmers in these regions the evolution of a new, virulent race of the pathogen,
an estimated $500 million in lost production alone and led changes in plantation management regimes promoting
to reduced production for at least two years [12, 13]. disease development and favorable weather conditions
Climate change threatens crop yields, both directly due to climate change [12]. Presently, coffee farmers from
through changes in plant growth and production and Colombia to Mexico are experiencing massive infestation
indirectly through impacts on crop diseases. It has been and as a result, big losses in yield. Recorded yield losses
estimated that changes in climate have already been from the Latin American region alone were 25% in the year
reducing global agricultural production by 1-5% per 2013 [25]. From Mexico to Peru farmers were experienced
decade over the last 30 years [14]. Climate change affects 40-50% reduction yield [25, 26]. Thus, the objective of this
pathogen biology not only directly but also indirectly review was to integrate climate variability and its effect on
through effects on host development and phenology. CLR diseases and to express the need for research in this
Climate change will influence the occurrence and area.
development of crop diseases and alter the geographical
distribution of pathogenic species [15, 16]. Milder winters Taxonomy and Phylogeny of CLR: The genus Hemileia is
could favor the cold-season survival of fungal foliar a member of the phylum Basidiomycota, class
pathogens and higher minimum temperatures could Pucciniomycetes, order Pucciniales (rust fungi). Currently,
generate early spring infections. However, an increase in more than 50 rust physiological races and 23 coffee
the variability of rainfall patterns will affect the pathogens differentials have been identified [10, 27]. Races are
differently, depending on whether they require free water attributed to isolates with distinct and unique
or saturated humidity to initiate the infection process combinations of virulence genes as inferred by Flor’s
[17, 18]. Many pathogens are likely to shift their gene-to-gene theory and described as sequential roman
geographic distribution through bioclimatic niche numerals in order of detection [28]. Thus, as no further
expansion or higher latitudes spread [19]. genetic confirmation has been possible so far, inferred
Recently CLR regained notoriety as the result of a rust race genotypes comprise virulence genes ranging
severe and widespread epidemic throughout Central from v1 to v9 in isolates derived from C. arabica and
America, Colombia, Peru and Ecuador, due to the tetraploid interspecific hybrids, while those of the races
World J. Agric. Sci., 17 (5): 418-429, 2021
420
that attack diploid coffee species are not known. generally favor propagation of leaf rust disease with a
Within the scale of coffee differentials, race II (v5) ratio of intensity that increases with the density of
presents the most restricted infection spectrum and is canopy [31].
considered the most common and widespread rust race in
the world, acquiring a generalized occurrence probably as CLR Life Cycle: The fungus begins its life cycle as a
a consequence of the uniform genetic background of most microscopic spore. Spores deposited on the underside of
C. arabica cultivars worldwide [29]. a coffee leaf during favorable weather conditions will
Epidemiology: The perennial nature of C. arabica and its stomata and growing, or colonizing the leaf, to extract
distribution around the equator ensures the presence of nutrients [39, 40]. Once the spores begin germinating, the
CLR throughout the year without a closed season unlike infection process usually is completed within 24 to 48
other rusts which undergo a period of survival [30]. hours, provided there is a continuous presence of
Genetically susceptible coffee plants in rust conducive moisture and the temperature ranges between 15 and
environments can be attacked at any growth stages [10]. 30°C. After infection, the fungus will grow and produce
However, since the spores of the pathogen germinate new spores in about three to four weeks [41]. The time
only in the presence of free water, epidemics are prevalent needed for germination, infection and the production of
during the wet season. new spores and the extent of the infection are largely
Rainy spells show an increase in the spread of the determined by weather conditions, particularly
disease and period of intense infection corresponds to temperature and moisture [38]. As other biotrophic
those of high rainfall [31]. Generally, the pattern of rainfall fungus, the infection process of H. vastatrix on coffee
determines the pattern of CLR development. In Kenya, to leaves involves specific events including appressorium
the east of Rift Valley, where there are two periods of formation over stomata, penetration into the leaf and
rainy seasons, the rust progress curve also had two colonization of living host cells by intracellular specialized
peaks as against one peak to the west of Rift Valley where fungal structures (haustoria) that penetrate the plant cell
there was only one season or rain was continuous [32]. wall and allow nutrient uptake.
In Ethiopia, onset of rust in monomodial rainfall at high
altitude is October to January with peak period in Symptom and Damage of Coffee Leaf Rust: The first
November to December while in lower altitudes rust symptom of coffee leaf rust disease is small discolored
increase from August to November with peak in spots which develop on the underside of the leaves.
September [33]. Other researchers reported the occurrence These small spots increase in size and are powdered with
of maximum rust incidence in November to December [34]. spores of the pathogen ranging in color from yellowish
When free water is present, the level of temperature orange to bright orange [31]. Observable symptoms are
determines the rate of germination and penetration small, pale yellow spots on the upper surfaces of the
processes. The seasonal and daily fluctuation in leaves. As these spots gradually increase in diameter,
temperature affects the rate of disease development. masses of orange urediniospores (= uredospores) appear
Within minimumand maximum limit, the lower and higher on the under surfaces. The powdery lesions on the
temperatures extend and reduce the latent periods, undersides of the leaves can be orange-yellow to red-
respectively. At very low temperature (< 10°C) and very orange in color and there is considerable variation from
high temperature (> 35°C) lesion enlargement is inhibited one region to another. While the lesions can develop
and often ends up as chlorotic lesion and perhaps anywhere on the leaf, they tend to be concentrated
completely inhibit infection [30, 35, 36]. around the margins, where dew and rain droplets collect.
Altitude influence local climatic conditions, which in The centers of the spots eventually dry and turn brown,
turn affect the development of the disease. CLR intensity while the margins of the lesions continue to expand and
was reported to decrease with altitude in Kenya [32], in produce urediniospores.
southern American continents [35] in Pauna New Guinea Early in the season, the first lesions usually appear
[36] and in Ethiopia [33, 37]. Coffee management practices on the lowermost leaves and the infection slowly
also influence the epidemics of CLR development. progresses upward in the tree. The infected leaves drop
According to Avelino et al. [38], the effect of coffee prematurely, leaving long expanses of twigs devoid of
management practices on infection is through variation in leaves. When a coffee plant does not have the optimal
fruit load of coffee trees and high yielding years are amount of leaf area, it does not have the ability to
generally conducive to rust infection. On the other hand, accumulate adequate energy via photosynthesis and
the humidity generated by the presence of shade trees store up the appropriate resources for fruit production.
germinate and infect the leaf, penetrating it through the
World J. Agric. Sci., 17 (5): 418-429, 2021
421
Fig. 1: Life cycle of Hemileia vastatrix. Drawing from: (www.apsnet.org/online/feature/edcenter)
In severe cases the fungus can present on young leaf pathogen threats. However, climate change and increased
buds or fruits. This is why there is generally a loss of climate variability are already available to assess the direct
yield even the year after rust outbreaks [38]. impacts of climate change on the distribution and
Climate, Weather and Coffee Leaf Rust: Climate change Climate influences the incidence as well as temporal
will influence the occurrence and development of crop and spatial distribution of plant diseases. The main
diseases and alter the geographical distribution of factors that control growth and development of diseases
pathogenic species [15, 16]. Milder winters could favor are temperature, light and water; similarly these factors
the cold-season survival of fungal foliar pathogens and affect type and condition of host crop [46, 47]. The
higher minimum temperatures could generate early spring environment may affect plant pathogen, therefore,
infections. However, an increase in the variability of survival, vigor, rate of multiplication, sporulation,
rainfall patterns will affect these pathogens differently, direction, distance of dispersal of inoculums , rate of
depending on whether they require free water or saturated spore germination and penetration can be affected
humidity to initiate the infection process [17, 18]. [48, 49].
Many pathogens are likely to shift their geographic Climate change will affect temperature, precipitation,
distribution through bioclimatic niche expansion or higher CO levels and frequency of extreme weather events, so
latitudes spread [19, 42]. Various factors could be put these will have a significant effect on agricultural
forward to explain the pace of pathogen emergence and production and the temporal and spatial distribution of
spread such as domestication of ecosystems and human pests and diseases [50]. Climate change will also affect
activities through trade and travel [43, 44]. Moreover, crop yields by altering rainfall and temperatures, but also
complex changes in crops and agricultural practices may by enhancing the growth of plant pathogens. Prior to the
result in future changes in both pathogen diversity and post-2011 CLR epidemic farmers considered small losses
importance of certain pathogens [19, 45].
2
World J. Agric. Sci., 17 (5): 418-429, 2021
422
Fig. 2: Influence of climate and weather variables on different CLR life cycle stages
Sources: Avelino et al. 2014
to CLR normal and expected. CLR was not problematic altitudes than ever before. Since 2012, Central America
above 1000 m. a. s. l until the post-2011 epidemic, when has been struck with an epidemic of coffee rust that is
CLR infestations of equal intensity were observed from badly damaging trees and undercutting local coffee-
400 to 1400 m a s l [12]. dependent economies. Rust has been in the Americas for
For example, rising temperatures threaten coffee tree over 40 years, but never affected more than 5% of the
plantations by boosting the fungal pathogen Hemileia crop. In 2013 the incidence was 53% [51].
vastatrix, infiltrates the leaves of coffee trees, defoliating Temperature plays a significant role in several
them and often killing the tree. However, because the lifecycle states, in addition to affecting pathogen survival
fungus cannot survive below 10°C, trees planted at higher and the plant’s ability to respond to the infection [52, 53].
elevations have historically been safe from this blight. Temperature most strongly influences germination and
“Until recently, rust only appeared below 1, 300 m infection (i.e. penetration and colonization). Specifically,
altitude; cooler temperatures protected higher altitude during germination, CLR is most affected by daily
plantings from the disease [51]. minimum and maximum temperatures, diurnal temperature
The primary weather-related variables that affect CLR variation (the difference between the high and low
include temperature, moisture and wind. These variables temperatures that occur during the same day) and the
influence CLR at difference stages in its life cycle: frequency of cold nights and warm days. Optimal
temperature affects germination, infection and the time temperatures for spore germination and infection are
required for the fungus to produce new spores; moisture between about 21 and 25°C [54, 55]. Temperatures below
(in the form of soil moisture, leaf wetness, or rainfall) 18°C and above 28°C delay the production of new spores
affects germination, infection and spore dispersal; and [41], while temperatures below 15°C and above 30°C more
wind primarily affects dispersal, though it can influence severely suppress germination and infection [30, 54, 55].
temperature and moisture as well. As average minimum temperatures (typically experienced
Temperature: Temperatures in tropical highlands are epidemics also increases. Conversely, the more frequently
increasing and this terrain is experiencing earlier and temperatures fall below the minimum threshold of 15°C,
heavier rainfall, allowing H. vastatrix to grow at higher the lower the infection rate and severity of CLR. With the
at night) increase, the incidence and severity of CLR
World J. Agric. Sci., 17 (5): 418-429, 2021
423
expectation that temperatures will continue to rise in the precipitation and thus decreased solar radiation and a
future, more areas at higher elevations likely will become narrower range between daily maximum and minimum
favorable to CLR [53]. temperatures [65]. These conditions led to more days
Since the last century, scientists have predicted with optimal conditions for CLR proliferation and
that global temperature would rise due to an increase in potentially to shorter periods between plant infection and
the concentration of greenhouse gases in the atmosphere the development of new spores that could infect plants
from natural and anthropogenic sources [14]. In the past [66].
150 years, the average surface temperature has
increased by 0.76°C and could increase from 2.4 to 6.4°C Moisture: Moisture plays a key role in the progress of
in the period of 2090-2099 relative to 1980 to 1999 [14]. CLR, affecting the germination, infection and spread of
High atmospheric CO concentrations, temperatures and spores and the overall health of the coffee plants [67].
2
changes in precipitation patterns as well as the frequency Although high humidity (greater than 80 percent) for
of extreme weather phenomena will significantly affect 24 hours or longer increases spore germination and rust
crop grow and production and therefore the presence of infection [68], humidity by itself in the absence of free
diseases will be altered under these conditions [56]. water is not enough [54, 67]. Free water on the leaves for
This change highlights the role climate has played in the at least six hours is necessary for spore germination and
CLR outbreak and will play in the future. Warmer infection, although germination alone can occur in as little
temperatures are expanding the range of CLR to higher as three hours if spores are fresh and conditions are
altitudes. Ghini et al. [57] observe that warmer minimum optimal and continuous leaf wetness for 20 hours is
temperatures contribute to a reduction in diurnal range, optimal for high infection rates greater than 80 percent
thus reducing the latency period for CLR and increases [54]. Additionally, the longer leaves remain wet, the
epidemic intensity. Reduction in diurnal range is a key and greater the severity of the disease and thus damage to the
consistent factor proceeding CLR epidemics [12]. Average plant [41]. Water also plays a critical role in the local
global surface temperatures have increased by nearly dispersal of CLR spores. When it rains, rust spores are
0.98°C in the century to 2015 GISTEMP [58], accompanied dislodged from leaves and carried in water droplets to
by significant changes in the dynamics of the oceans and other leaves on the same plant or sometimes to other
atmosphere IPCC. Wild populations of plants and animals plants. This mechanism is known as “rain splash” and is
have shifted their geographical ranges and phenologies responsible for CLR spore dispersal over short distances
in response [59] and changes in crop–pathogen [69].
interactions mediated by altered climates are thus a Changes in the onset of rainy seasons may also
reasonable expectation [60, 61]. affect CLR and plant health, where early onset of rains
Increase in temperatures with sufficient soil moisture may extend the growing season for CLR and late onset
may increase evapo-transpiration resulting in humid may stress plants, making them more vulnerable to
microclimate in crop and may lead to incidence of diseases diseases [66]. CLR outbreaks in Latin America in recent
favored under these conditions [62]. As the temperature years have been associated with an earlier onset of the
increases, the duration of winter and the rate of growth rainy season and also may have allowed CLR to
and reproduction of pathogens may be modified [63]. proliferate more than in previous years [66].
Drought and temperature stress have been shown to
negatively affect a plant’s ability to respond to biotic Wind: Wind plays an important role in spore dispersal
stresses via changes in endogenous abscisic acid levels and may also affect leaf wetness and overall plant health.
that affect defense responses involving salicylic acid, Wind needs to be sufficiently strong (greater than about
jasmonic acid, or ethylene [64]. 7mph) to dislodge spores from leaves and transport them
CLR outbreaks in Colombia in 2012–2013 have been to other plants and higher speed winds tend to transport
attributed in part to above-normal minimum temperatures larger quantities of spores than slower winds [70].
and below-normal maximumtemperatures [65]. This period Wind can also affect plant health. Storms and hurricanes
was associated with La Niña conditions; for Colombia, often severely damage coffee trees and reduce coffee
other parts of northern South America, Central America yields [71]. Plants that are stressed by storm damage may
and the Caribbean, that meant increased cloud cover and be more susceptible to CLR and other disease.
World J. Agric. Sci., 17 (5): 418-429, 2021
424
In general, high moisture and temperature must be played an important role in spore dispersal over both
favorable and act together in the initiation, development short and long distances.
of plant diseases, as well as germination and proliferation
of fungal spores of the vast majority of pathogens [47]. CLR Disease Management: Several factors may strongly
Due to changes in temperature and precipitation influence coffee rust epidemics such as: shade status,
regimes, climate change may alter the growth stage, coffee tree density, fertilization and pruning since they
development rate and pathogenicity of infectious agents produce effects on microclimate and plant physiology
and the physiology and resistance of the host plant [72]. which, in turn, influence the life cycle of the fungus.
A change in temperature may favor the development of These factors should be considered in crop management
different inactive pathogens, which could induce an depending if coffee is cultivated in intensive or extensive
epidemic. plantation [38].
Other Factors Influencing CLR: In addition to climate Disease Resistance Breeding: Breeding coffee plants for
and weather, a number of other factors related to resistance to rust is considered the best disease
agricultural practices and other environmental stressors management strategy both environmentally and
influence incidence and severity of CLR in any given economically [11]. The first effective effort to select
place or time. These include coffee plant exposure to resistant germ plasm was conducted in India in 1911,
shade or sun, the density of coffee plants, the amount of giving rise to the release of the cultivar ‘Kent’s’, which
viable CLR spores remaining from the previous year, soil replaced the susceptible cultivar ‘Coorg’ [10]. Several
quality and human dispersal of spores. Additionally, some missions to Ethiopia were subsequently conducted,
varieties of coffee particularly Arabica are more but no effective resistance sources were identified [10].
susceptible to infection than others. Shade can create In the 1950s, concern for the potential introduction of
optimal temperature and moisture conditions for CLR, with rust into the American continent led F. Wellman and W.
the exception of dew, which tends to be less prevalent in Cow gill to conduct field missions in the Eastern
shade [38], but has differing effects on spore dispersal Hemisphere, collecting more than 100 coffee types new to
depending on moisture conditions. Shade suppresses the Americas. In collaboration with Branquinhod’ Oliveira,
CLR by decreasing stomatal density [38], which creates the work of these researchers led the USA and
optimal conditions for another fungus, Lecanicillium Portuguese governments to provide financial support
lacanii, a natural parasite of the CLR fungus [73] and by for the creation of the Coffee Rusts Research Center
reducing coffee crop yield [67, 74]. Higher yield, or “fruit (CIFC, Centro de Investigação das Ferrugens do Cafeeiro)
load, ” is associated with higher incidence of CLR and in Portugal, located far from coffee-growing regions and
because fruit loads tend to be lower under shade, shade thus centralizing research on CLR at the international
can reduce the incidence of CLR [67, 74]. When berries are level. Since 1955, CIFC has received and characterized
removed before they ripen, the severity of the infection coffee and rust germplasm and supplied breeding
decreases, possibly because the plants can contribute programmes at coffee research institutions with
more toward resistance instead of fruiting [35]. characterized resistance sources, along with scientific and
Leaves in full sun are more susceptible to CLR than technical information and training. HDT (Híbrido de
leaves in the shade [75]. Conversely, shade can increase Timor) populations derived from a plant discovered on the
the incidence and/or severity of CLR by reducing solar island of Timor in 1927 exhibiting resistance to rust among
radiation reaching the coffee plants and increasing leaf ‘Typica’ coffee crops [29]. In the 1950s, these populations
size, which increases the surface area of leafs onto which were shown to be natural hybrids between C. arabica and
CLR spores can land [38]. C. canephora, most of them offering resistance to all rust
Farms with high coffee plant density tend to races known at that time [10]. The importance of HDT
experience more frequent and severe disease outbreaks populations as resistance sources relies on the long
[35], possibly because the rust spores are easily durability of some of these resistance factors, which in
transmitted from one plant to another, making control some cases resistances have been in use for more than
difficult [76].Although wind and rain splash are important 30 years. In Ethiopia 8136, 7516 and 1579 coffee cultivars
dispersal mechanisms of CLR spores, humans have also showed resistant reaction for CLR [77].
World J. Agric. Sci., 17 (5): 418-429, 2021
425
Biological Control: With coffee rust insects, mites and conducted with systemic fungicides (e.g., epoxiconazole,
various fungal species have been reported. Insects and pyraclostrobin). The combined or alternate use of copper-
mites may reduce rust spore load through direct feeding based and systemic fungicides is advised to avoid the risk
of the urediniospores but could also be important of selecting fungicide-resistant rust populations [41].
disseminators of urediniospores [78]. Among fungal
species reported as hyperparasites, Verticillium lecanii CONCLUSIONS
is the most common ones occurring in many countries. H.
vastatrix spores are hyperparasitised by the Ascomycete In spite of its destructiveness, worldwide distribution
fungus Lecanicillium lecanii. Although unable to and economic impact on the production of such an
effectively control CLR, this hyperparasite is capable of important cash crop as coffee, Hemileia vastatrix has not
reducing spore viability and disease severity [25]. been as widely studied as other rust fungi. The ability of
Lecanicillium lecanii is primarily an entomopathogen of farmers to manage CLR requires identifying early signs of
the green coffee scale Coccus viridis, which in turn has a the disease and being able to respond accordingly.
mutualistic association with the arboreal nesting ant Understanding the climate and weather connections to
Azteca instabilis. The relationships between these CLR outbreaks may allow farmers to prepare for and
organisms suggest that complex ecological interactions manage the disease more effectively and ultimately reduce
may play an important role in disease incidence and crop losses. Understanding the climate CLR connection
severity, potentially explaining why CLR is sometimes a is especially important given that global climate change is
severe epidemic and other times a troublesome but not likely to affect the incidence and severity of the disease in
devastating problem [25]. A significant reduction in leaf the near future. Generally, further research will be focused
rust severity by the presence of Verticillium psalliotae, on discovering climate change adaptation strategies
especially when was applied 24 hours before the feasible for smallholder producers for practically
inoculation of H. vastatrix, demonstrated an evidence implement.
parasitism in vivo [79]. It has been showed that the
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