Multiple-Disease System

PY56CH27_Avelino ARI 29 June 2018 14:15
Annual Review of Phytopathology
Multiple-Disease System
in Coffee: From Crop Loss
Assessment to Sustainable
Access provided by University of California - Santa Barbara on 07/11/18. For personal use only.
Management
Annu. Rev. Phytopathol. 2018.56. Downloaded from www.annualreviews.org
Jacques Avelino,1,2,3 Clémentine Allinne,2,4

Rolando Cerda,2 Laetitia Willocquet,5
and Serge Savary5
1
CIRAD, UPR Bioagresseurs, 30501 Turrialba, Costa Rica. Bioagresseurs, Université de
Montpellier, CIRAD, 34090 Montpellier, France; email: jacques.avelino@cirad.fr
2
Program of Sustainable Agriculture and Agroforestry, Centro Agronómico Tropical de
Investigación y Enseñanza (CATIE), 7170 Turrialba, Costa Rica; email: rcerda@catie.ac.cr,
javelino@catie.ac.cr, callinne@catie.ac.cr
3
Inter-American Institute for Cooperation on Agriculture (IICA), 11101 Coronado, San José,
Costa Rica
4
CIRAD, UMR SYSTEM, 30501 Turrialba, Costa Rica. SYSTEM, Université de Montpellier,
CIHEAM-IAMM, CIRAD, INRA, 34090 Montpellier SupAgro, Montpellier, France;
email: clementine.allinne@cirad.fr
5
UMR AGIR, Institut National de la Recherche Agronomique (INRA), Université de Toulouse,
INPT, INP-EI Purpan, Castanet-Tolosan, France; email: serge.savary@inra.fr,
laetitia.willocquet@inra.fr
Annu. Rev. Phytopathol. 2018. 56:27.1–27.25 Keywords

The Annual Review of Phytopathology is online at agroforestry system, Coffea arabica, crop health, ecosystem service, injury
phyto.annualreviews.org
profile, primary and secondary yield losses
https://doi.org/10.1146/annurev-phyto-080417-
050117 Abstract
Copyright c 2018 by Annual Reviews. Assessment of crop loss due to multiple diseases and pests (D&P) is a neces-
All rights reserved
sary step in designing sustainable crop management systems. Understand-
ing the drivers of D&P development and yield loss helps identify leverage
points for crop health management. Crop loss assessment is also necessary
for the quantification of D&P regulation service to identify promising sys-
tems where ecosystem service provision is optimized. In perennial crops,
assessment of crop losses due to D&P is difficult, as injuries can affect yield
over years. In coffee, one of the first perennials in which crop loss trials
27.1
Review in Advance first posted on
July 11, 2018. (Changes may still
occur before final publication.)
were implemented, crop losses concurrent with injuries were found to be approximately 50%
lower than lagged losses that originated following the death of productive branches due to D&P.
Crop losses can be assessed by field trials and surveys, where yield reduction factors such as the
number of productive branches that have died are quantified, and by modeling, where damage
mechanisms for each injury are considered over several years.
INTRODUCTION
Coffee is a major traded commodity for the developing world, second only to oil in financial terms
(129). According to the International Coffee Organization, the total production by all exporting
countries was 8.88 million tons of green coffee in the coffee harvest year 2015/2016 (58). Total
exports in that year reached 6.71 million tons, worth approximately US$17.7 billion (58). The
importance of coffee in terms of foreign exchange often hides the social and economic relevance
of the crop within these producing countries. A large fraction of the world population has some
relationship to the coffee sector, from farmers and farm laborers, processors, exporters, importers,
roasters, and retailers to consumers. Approximately 125 million people worldwide depended on
coffee in 2002 for their livelihoods (84), including 25 million producers (87). Any event affecting
coffee production and/or coffee prices could potentially impact the livelihoods of millions of
people, as has been demonstrated during the severe coffee rust epidemics in Latin America from
2008 to the present (6, 72).
Coffee is exposed to many diseases, pests, and weeds. Although most studies on coffee health
have focused on individual diseases, the coffee crop is often affected by several diseases simul-
taneously (1, 29, 30, 62, 110). Disease(s) and pest(s) (D&P) are commonly associated and can
interact, because pathogens and pests have the same biophysical requirements or because in-
jury by one enhances (or suppresses) the other (110). For instance, defoliation due to the fungus
Hemileia vastatrix, which causes coffee leaf rust (CLR), is often aggravated by other leaf diseases,
such as brown eye spot (BES) due to Cercospora coffeicola and anthracnose due to Colletotrichum
gloeosporioides, and ultimately by branch dieback, which is itself aggravated by a complex of op-
portunistic fungi (142). These diseases are typical in trees weakened by the defoliation caused by
CLR and also contribute to yield and quality losses. Crop loss assessments should consider the
D&P complex because of the many interactions between (1) the dynamics of injuries and (2) the
dynamics of the effects of these injuries on crop physiology (74, 112).
Quantification of crop losses caused by D&P is a necessary first step toward crop health man-
agement (112). For instance, one of the reasons why the economic responses (bank loans, actions
by funding agencies) to the recent coffee rust crises in Central America were delayed was the lack
of information on crop losses (6). Crop loss information is also necessary for the quantification
of the regulation service of D&P (9, 29, 30), an important step toward the design of optimized
management systems in which the provision of ecosystem services (ESs) is amplified, particularly
D&P regulation (100).
This review aims to show how the consideration of the multiple-disease system in coffee, as a
model system for perennial crops, can help in designing sustainable crop management based on
crop loss assessment. We will focus on the main cultivated coffee species, Coffea arabica.
COFFEA ARABICA
The genus Coffea is endemic to Africa and comprises more than 130 recognized species (3).
However, due to consumption preferences, history, and diseases, only two main coffee species
27.2 Avelino et al.
are cultivated today. C. arabica (Arabica) stands first, representing 63.5% of the exports in the
2015/2016 coffee year (58). The second species is Coffea canephora (Robusta), representing almost
36.5% of world production in the same coffee harvest year. A third species, Coffea liberica (Liberica),
is marginal, with a share of world production below 1%. Arabica commands the highest prices
due to its higher quality.
C. arabica originates as an understory plant in the rainforests of a reduced territory in the
Ethiopian highlands, in cool areas (3, 56, 143). It is autogamous and the only allotetraploid Coffea
species (others are diploid): 2n = 4X = 44. This species seems to come from a recent and probably
unique event of hybridization between two diploid species, C. canephora and Coffea eugenioides (63).
As a result, C. arabica has a low genetic diversity. Much of the work by breeders involves increasing
the diversity among cultivated cultivars to better confront issues such as those caused by climate
change: increase of threats from D&P and decrease of coffee yield and quality (133).
COFFEE-BASED AGROFORESTRY SYSTEMS AND THE ECOSYSTEM

SERVICES GENERATED
C. arabica is a shade-adapted species (27, 36) that is now cultivated from monoculture plantations
under full sun exposure to a wide range of agroforestry systems (AFSs), including monospecific
shade systems, other AFSs with diversified shade trees, and even complex forest-like agroforests
(Figure 1). AFSs generate ESs (1, 29, 30, 32, 64, 100, 102, 125, 130, 131) that are essential to
system sustainability and may impact D&P development. These services fall within the four broad
groups of ESs defined by the Millennium Ecosystem Assessment (75): provisioning, supporting,
regulating, and cultural services. This diversity of ESs generated by AFSs contributes to several
economic, social, and ecological attributes that generally improve their sustainability over that of
monocultures (17, 29, 30, 64, 130, 131).
Shade trees provide habitats for a great number of species, including birds, ants, and fungi (64,
89, 128, 130), with potential for the regulation of D&P. Shade trees also dampen microclimatic
extremes: air, leaf, and soil temperatures are buffered; wind speed and solar radiation are reduced;
and soil moisture fluctuations can also be diminished (85); however, relative humidity of air and
plant organ wetness are increased (10, 13, 17, 36, 66, 68, 69, 121). Shade trees intercept light,
thereby suppressing weeds, especially aggressive grassy weeds (17, 124, 128). AFSs also contribute
to carbon sequestration in the plant species they harbor and in soil (30, 77). Shade trees in AFSs
can provide additional regulating services by reducing surface runoff and soil loss (46, 136). AFSs
also improve water quality and enable a regular provision of water for human consumption or
hydroelectricity production (46, 67, 96).
Complexity of structure and composition
Monoculture Association with other trees Close to natural ecosystems
Figure 1
Gradient of complexity in coffee-based agroforestry systems. Photographs provided by Clémentine Allinne.
www.annualreviews.org • Multiple-Disease System in Coffee 27.3

In addition to coffee production, coffee-based AFSs produce other provisioning services. AFSs
contribute to farmers’ livelihoods in the form of food, fuelwood, and construction materials (17,
32, 102). These products diversify incomes, thereby reducing economic dependence on the main
coffee crop (17, 102). The microclimate in AFSs influences the coffee plant physiology, its yield,
and coffee quality. Shade trees stabilize yield over years (27, 36), resulting in more stable income
to growers. High solar radiation leads to high coffee yield. However, high production by a tree
in a season leads to a reduced branch growth and even diebacks and reduces productivity in the
following one. The result is a biennial yield behavior, with particularly high amplitudes in unshaded
coffee systems (27, 36). Shade generated by trees intercropped with coffee also favors coffee quality
by suppressing excessively high yields and increasing the duration of berry maturation due to
buffered temperatures (82, 132). Effects on both yield stability and quality contribute to increased
provisioning services over the long-term.
AFSs also improve their own environmental resources (17, 51) by (a) reducing (improving)
soil acidity and increasing its bases’ content, particularly potassium, through organic matter (30,
51, 52); (b) providing nitrogen, for example, in leguminous tree associations, where the litter fall
and pruning residues can produce up to 340 kg of nitrogen per hectare per year (17, 51); or
(c) increasing soil biodiversity as earthworm populations (38, 52).
Finally, AFSs are the basis for other activities, such as ecotourism, that contribute to the
protection of complex, traditional, and culturally established AFSs (130).
MAIN DISEASES AND PESTS OF ARABICA COFFEE

Coffee D&P can cause different yield and quality losses depending on the organ affected and on
the dynamics of damage (Figure 2). D&P may produce primary losses by reducing the yield (and
quality) in the year of the epidemic and secondary losses in the following years (150).
Only one major coffee disease appears to have worldwide distribution (Table 1): CLR, caused
by H. vastatrix. CLR is specific to Coffea spp. The disease can cause heavy defoliation and death of
branches, resulting in primary and secondary losses. CLR originated in Africa, as does coffee, and
was at the center of concerns in Latin America before 1970, when it was introduced into Brazil.
At that time, all Latin American coffee areas were planted with cultivars that were genetically
very homogenous and susceptible to CLR. The risk of epidemic was thus high, analogous to
the island of Ceylon, where coffee stands were destroyed by the pathogen at the end of the
nineteenth century (71, 117, 146). However, shortly after its appearance in Latin America, the
disease, which was managed mainly by fungicides, was not viewed as a threat anymore. CLR
reemerged in 2008 in Colombia; in 2012 in Central America, Mexico, and the Caribbean; and in
2013 in Peru and Ecuador. In Colombia, CLR caused an average decrease in production of 31%
from 2008 to 2011 compared with 2007 (6). In Central America, production decreased by 16%
in the 2012/2013 harvest, the year of the epidemic, compared with 2011/2012, and by 21% in
the following year (59). The resurgence of the disease has been attributed to a combination of
economic and meteorological factors: low coffee profitability, leading to a suboptimal management
of the plantations, and an increase of minimum temperatures, possibly reducing the latent period
of the disease (6). However, in Colombia, changes in temperature and leaf wetness from 2008 to
2011, favoring the infection process, were discarded by Bebber et al. (15). No differences were
found between these CLR years and years with no CLR. In tropical environments, necessary
conditions for CLR infection are often met during the night—particularly wetness, which is not
limiting, due to dew deposition (6, 68).
Other important coffee diseases are restricted to either Africa or Latin America (Table 1).
Mycena citricolor is the causal agent of American leaf spot disease (ALSD) in coffee. This is a new
27.4 Avelino et al.

a Dieback
Trunk,
Necrosis and branches
leaf drop Flower rot and
berry drop
Number of fruiting nodes Necrosis
Lesions Leaf area
Number of fruits per node
Root Bean weight
Actual
Reserves
yield
Year n
Injuries physiological impacts
b Dieback Primary yield losses

Secondary yield losses
Trunk,
Necrosis and branches
leaf drop
Number of fruiting nodes

Lesions Leaf area
Root Bean weight
Actual
Reserves
yield
Year n
Trunk,
branches
Number of fruiting nodes

Leaf area
Root Bean weight
Actual
Reserves
yield
Year n + 1
Figure 2
Conceptual representation of physiological damage due to diseases and pests on coffee yield over years and of (a) primary and (b)
secondary yield loss pathways (150). In coffee, the yield components are the number of fruiting nodes per tree, number of fruits per
node, and bean weight. By reducing leaf area—via leaf necrosis, leaf drop, and death of branches (dieback)—foliar disease and pest
injuries alter the source–sink relationships and reduce the number of fruits per node and the bean weight. These two components are
also directly reduced by fruit drop and berry necrosis. The physiological damages affect that year’s yield, resulting in primary yield
losses. Leaf area reduction and dead branches decrease the translocation process toward the branch tips and the branch growth,
decreasing the number of fruiting nodes per tree in the following year, resulting in secondary yield losses.

Table 1 Main Arabica coffee diseases and pests in coffee-producing regions and main organs affected
Susceptible Worldwide Latin America and the Asia and
organ distribution Caribbean only Africa only Oceania only References
Leaf Coffee leaf rust, fungus American leaf spot Leaf miner, insect pest: NA 44, 56, 81,
pathogen: Hemileia disease, fungus Leucoptera meyricki 122,
vastatrix pathogen: Mycena 142–144
citricolor (Omphalia
flavida)
Leaf miner, insect pest:
Leucoptera coffeella
Flower, Coffee berry borer, American leaf spot Coffee berry disease, NA 37, 44, 56,
fruit insect pest: disease, fungus fungus pathogen: 81, 122,
Hypothenemus hampei pathogen: Mycena Colletotrichum kahawae 135, 143,

citricolor (Omphalia Antestia bug, insect pest: 144
flavida) Antestiopsis spp.
Trunk, Branch dieback, NA Coffee wilt disease, Asian white 42, 44, 45,
branch physiological disorder: fungus pathogen: stem borer, 53, 56, 81,
several causes, Gibberella xylarioides insect pest: 106, 107,
including overbearing, (Fusarium xylarioides) Xylotrechus 143, 144
heavy defoliation due African white stem quadripes
to diseases and pests, borer, insect pest:
and opportunistic fungi Monochamus leuconotus
Root NA Root-knot nematodes: NA Root-lesion 26, 57, 126,
Meloidogyne spp. nematodes: 137, 143
Pratylenchus
spp.
Abbreviation: NA, not available.
encounter disease of coffee in Latin America. M. citricolor has a broad range of hosts, including
shade trees used in coffee plantations as well as weeds (48, 119). When conditions are favorable—
that is, when rainfall is abundant and homogeneously distributed in the year and temperatures are
cool (5)—yield losses in coffee plantations can be almost complete (145). M. citricolor infects leaves,
fruits, and branches. Injuries on the foliage are the most serious since they can result in severe
defoliations and branch deaths, causing high primary and secondary yield losses. Injuries on fruits
can cause them to drop and result in high primary yield losses. Injuries on branches are less frequent
and have no serious impact on yield. The last severe epidemic at the Central America–Colombia
regional scale occurred in 2010 (48). Coffee berry disease (CBD) and coffee wilt disease (CWD,
or tracheomycosis) are two other serious coffee diseases, reported only in Africa. CBD is caused
by Colletotrichum kahawae, while CWD is caused by the Fusarium xylarioides teleomorph Gibberella
xylarioides (Table 1). C. kahawae is specific to C. arabica. The pathogen can infect flowers, fruits,
leaves, and even maturing bark (56, 122). The economic impact results from a massive drop of
infected green berries. Yield losses up to 80% have been reported (56, 122). CBD is a permanent
threat to high-elevation Arabica coffee crops, where cool temperatures and high humidity favor
infections (140). F. xylarioides causes a lethal vascular wilt of coffee due to the obstruction of the
xylem vessels and the disruption of water supply to the aerial organs (45, 56, 107). Infection leads
to the death of the tree within a period that varies from a few weeks to six months (53, 106, 107).
Uprooting and replacement of dead plants are common practices, although they are often only
temporarily effective (45, 91). In the first half of the twentieth century, the disease was considered
27.6 Avelino et al.

the most important coffee disease in Central and West Africa, where it destroyed almost all of
the C. liberica and part of the C. canephora stands (106). However, the disease began to decrease
in importance from the late 1950s, due to the uprooting of dead plants and their replacement
with resistant C. canephora cv. Robusta trees. CWD reemerged on Robusta in the Democratic
Republic of Congo at the beginning of the 1970s and then spread toward Eastern Africa. This
situation was possibly due to the evolution of the pathogen or the reemergence of a virulent strain
that initially went unnoticed and the overcoming of host plant resistance in Robusta genotypes.
Arabica-specific strains of F. xylarioides have been known in Ethiopia since the late 1950s, but it is
only recently that the disease caused important damages and major concerns (45, 56, 106, 107).
The importance of parasitic nematodes in coffee-based AFSs is presumably underestimated,
given the difficulty of detecting and assessing injuries and the expertise required to correctly iden-
tify their causation. The impact of nematodes has been documented in Latin America, particularly
in Brazil and Central America, and in Asia. In Latin America, the root-knot nematodes (RKNs)
Meloidogyne spp. are considered the most important nematodes. The main Meloidogyne species are
Meloidogyne exigua, Meloidogyne incognita, and Meloidogyne paranaensis (26, 126). However, in Asia,
the root-lesion nematodes (RLNs), Pratylenchus spp., are generally considered as dominant (26)
(Table 1). Pratylenchus coffeae and Pratylenchus brachyurus are the most widespread species (57).
Production of nematode-attacked coffee trees gradually declines, suggesting important secondary
yield losses. However, when environmental conditions are adverse for the coffee tree, yield losses
can be heavy from the very first high-fruit-load year when demand for nutrients is high, causing
early and heavy branch diebacks and even the death of the coffee trees (137–139). Complex diseases
involving Meloidogyne spp. and Fusarium oxysporum also occur (126): for example, the corky-root
disease, a combined infection by Meloidogyne arabicida and F. oxysporum, has been reported to cause
severe injuries leading to plant death in fewer than four years in Costa Rica (19, 126).
Dieback of branches is a common injury caused by a complex syndrome that is widespread
at a global level (Table 1). This syndrome, which results in heavy primary and secondary yield
losses, is related to physiological imbalances due to an excess of fruits (overbearing disease),
heavy defoliation due to D&P such as coffee rust or nematodes, and stresses such as heat shocks.
Opportunistic fungi, a dominant one being C. gloeosporioides, may aggravate this physiological
problem (34, 42, 81, 143). Lesions on leaves and berries due to C. gloeosporioides are also often visible.
C. arabica is affected by a number of insect species, the most important and widespread being
the coffee berry borer (CBB), Hypothenemus hampei (Table 1). This insect is very specific to coffee,
although adults may occasionally infest other plants (37). The fertilized female bores a hole in the
coffee berry and lays its eggs in the coffee endosperm, which is consumed by larvae. Only one of the
two beans of the coffee fruit is usually attacked. Primary yield losses result from a yield reduction
due to insect galleries and bean consumption by the insects and to the drop of young green fruits
deemed unsuitable for infestation, which fall after being probed and abandoned by the CBB (37,
44, 135, 143). The coffee quality is affected in three aspects: (a) holes and galleries in the bean
cause a decrease in physical quality; (b) development of undesirable flavors from infested and often
rotten beans negatively impacts organoleptic quality; and (c) CBB infestation constitutes a sanitary
issue since the bored beans may contain fungal toxins, including the ochratoxin A, a nephrotoxic
and carcinogenic toxin produced by Aspergillus ochraceus (101). The antestia bugs (Antestiopsis spp.)
constitute another pest in Africa that mainly affects fruits. These insects feed on green berries and
flower buds, causing primary yield losses through fruit drop and flower rot. However, antestia bugs
also negatively impact coffee quality by facilitating the introduction of Pantoea coffeiphila sp. nov., a
bacterium that produces the so-called potato taste due to pyrazine molecules (50, 101). Leaf miners
(LMs) of the genus Leucoptera are particularly problematical in Brazil and East Africa (Table 1).
These moths lay their eggs on the upper leaf surface. The larvae chew the leaf tissue, forming

galleries and lesions. Reduction in photosynthetic area and heavy defoliations can result from these
injuries, leading mainly to secondary yield losses (44, 143). Two stem borers are also serious pests
of C. arabica: Monochamus leuconotus in Africa and Xylotrechus quadripes in Asia (Table 1). The main
injuries are ring barking and the building of galleries in the wood by the larvae, which interrupts
the vascular transport. The effects are wilting, defoliation, shoot diebacks, and the death of stems
and trees (44, 143), causing high primary and secondary yield losses.
PRODUCTION SITUATIONS IN COFFEE

The dynamics and consequences of D&P are dependent on production situations (PSs) (1, 11, 29,
110, 115, 148)—that is, on the specific biophysical and socioeconomic context in which agricultural
production takes place (24, 88, 97, 110, 112). Knowledge of the relationships that link D&P to PSs
provides an understanding of the main factors influencing D&P development and helps identify
leverage points for action toward crop health. The concept of a PS has been particularly used
in crop-loss analysis by comparing the attainable yield, which is the yield obtained in a given PS
with no D&P, with the actual yield, obtained in the same PS when D&P occur (111–114, 150).
Three important crops, among others, and their pathosystems have been studied from the PS
perspective: rice (111, 114, 115), wheat (148), and coffee (1, 11, 29).
Coffee is grown in diverse shade conditions, which modify the environment (physical, biologi-
cal) of the crop and its D&P and therefore their physiology and development (1, 11, 29, 30). A coffee
PS can then be defined as a system (97) where interactions occur between (a) a coffee population
with its characteristics (cultivar, planting density, plant age, height), (b) the intercropped peren-
nial shade trees and annual weeds, (c) the biological and physical environments (soil, mesoclimate,
topography, landscape), and (d) the cropping practices, all associated with a given socioeconomic
context. Because some of these characteristics may vary with production years, particularly crop-
ping practices, it has been proposed that even for perennial crops, a PS could be centered on only
one year (1, 11, 29) (Figure 3). This annual conception of a PS in perennial crops also helps isolate
plant growth dynamic and polyetic effects (150) on D&P—effects from one year to subsequent
ones. Polyetic effects have been emphasized in the case of CLR (10), whose intensity in a given
year is dependent on the intensity in the previous one. CLR often has a biennial pattern that
follows the biennial cycle of coffee production. This is related to the reduced field resistance of
coffee plants to CLR when the expected yield is high (8, 10, 11, 68, 151) and to the high secondary
yield losses caused by the disease (31). PS approaches in coffee-tree pathology have been used to
study one disease, CLR (11), and more recently, multiple D&P along with provision of ESs (1,
29) and crop loss assessments (29).
EPIDEMIOLOGY OF COFFEE DISEASES

The physical environment and crop management are the main PS components driving coffee
diseases (Table 2). Most coffee pathogens have temperature requirements that determine their
distribution as a function of altitude (Table 2). For instance, CLR, ALSD, CBD, and phoma
leaf blight (PB), caused by Phoma costarricensis) could be tentatively ranked in this way according
to their altitude preference, from low to high (5–7, 21, 25, 56, 65, 81, 83, 90). The amount and
distribution of rainfall are also important factors influencing coffee diseases. CLR and ALSD
seem to be particularly dependent on rainfall distribution (Table 2). CLR appears to be reduced
by rainy seasons with continuous rainfall, which contribute to the elimination of its propagules
(6, 109), whereas ALSD is lessened when the rainy season is interrupted by dry spells, which
contribute to the desiccation of the propagules (5). Other diseases seem more strongly related to
the nutritional status of the coffee plant, such as BES (Table 2) caused by C. coffeicola, which behaves
27.8 Avelino et al.

Plot biophysical characteristics

Environment
Plant biodiversity,
Attainable yield
structure, and
Socio- composition
economic Injury
conditions Shade Actual yield
profile
Coffee
Weeds
population
Crop
management
Soil
Year n, PS 1
Plot biophysical characteristics

Environment
Plant biodiversity,
Attainable yield
structure, and
Socio- composition
economic Injury
conditions Shade Actual yield
profile
Coffee
Weeds
population
Crop
management
Soil
Year n + 1, PS 2
Figure 3
Conceptual representation of a coffee-based agroforestry system from the production situation (PS)
perspective. A PS is the biophysical and economic context in which production takes place (24, 88, 97, 110,
112). As contexts can evolve, each year leads to a different PS (PS 1 and PS 2), even in a perennial crop such
as coffee. The attainable yield is that obtained in a specific PS with no pests or diseases. The actual yield is
that obtained in a specific PS exposed to an injury profile, that is, a given combination of injury levels caused
by a range of diseases and pests (1, 29, 110–114, 150).
as a weakness parasite and is favored in conditions of low nitrogen supply (28). Soil characteristics
appear important for some coffee diseases. RKNs (Table 2) prefer sandy soils with low organic
matter content (4, 54). Sandy soils provide adequate moisture and facilitate nematode migration
(95, 120), and organic matter promotes beneficial organisms (147). In addition, increased levels of
CLR have been associated with acidic soils (11, 62), supporting observations made in 1956 about
high levels of CLR related to nutrition issues (35).
Crop management, including crop health management, is a reflection of the environmental,
economic, and social contexts of farmers’ decision making (23, 60, 73). As in other perennial crops,
such as apples (60), most D&P in coffee are thus dependent on socioeconomic factors. However,
these relationships are not well documented in coffee, with the exception of CWD, whose spread
over medium to large distances has been related to the use of wood for cooking and heating;
wood of dead coffee trees, where propagules can be produced over a long time, is used and sold
for that purpose (45, 53, 107). Among cropping practices, direct control methods have obvious
consequences on disease levels, but other practices can also have strong effects. Intercropping with
shade trees, in particular, has been reported to favor CLR (65, 68, 128), ALSD (5, 32), and thread

Table 2 Main drivers of Arabica coffee diseases on susceptible coffee trees

PY56CH27_Avelino
Topography/
Disease and pathogen temperature Rainfall/wetness Shade/light Socioeconomic factors Other factors
ARI
Diseases of primary importance
27.10
Coffee leaf rust: Low-altitude disease (7, Rainfall contributes to Higher incidence/ Low coffee profitability, Higher severity and
Hemileia vastatrix 21, 25, 65): <1,400 uredospore wash-off occurrence under shade thus low investment in incidence on high-
MASL in Guatemala in (109) (65, 68, 128) stands, helps explain yielding coffee trees
29 June 2018
2012 (6) High incidences when past great epidemics in (8, 10, 11, 68, 151)
Avelino et al.
Optimum range of rainy season is humid Colombia and Central Effective dispersal by
temperature is enough, favoring America (6) laborers (16)
14:15
21–28◦ C (142) infection, but

interspersed with bright

days, reducing
uredospore wash-off
(6, 70)
American leaf spot Medium-altitude High incidence when the Higher incidence under Often found in Many hosts within shade
disease: Mycena disease: 1,100–1,550 rainy season has no shade (5), particularly smallholders’ plots with trees and weeds of the
citricolor (Omphalia MASL in Costa Rica in interruption (5) when provided by tall suboptimal coffee agroecosystem
flavida) 2002–2003 (5) trees (5, 32); raindrops management and no (48, 119)
High incidence in of higher kinetic coffee tree pruning
western-oriented energy under shade activities (tall coffee
slopes (5) trees may promote the trees promote the
dispersal of the heavy disease due to
propagules (32) self-shading) (5)
Coffee berry disease: High-altitude disease High incidence positively Incidence/occurrence is No specific information Incidence dependent on
Colletotrichum kahawae (56, 83): ∼1,500 MASL related to the number of reduced under shade found flowering dates (49)
in Northern Malawi in rainy days (49, 78, 79) (65), possibly due to with escape possibilities
1998–1999 (90); Wet conditions promote raindrop interception through early
1,700–1,900 MASL in sporulation and dispersal (80) or temperature irrigation, stimulating
Uganda in 2014 (65) (141) regulation (83) flowering in dry
Optimum range of periods (81)
temperature is
17◦ C–28◦ C (83)
Incidence increases with
decreasing
temperatures (79)
(Continued)
Table 2 (Continued)
PY56CH27_Avelino
Topography/
ARI
Coffee wilt disease: No specific information Perithecia as well as conidia Shade increases the Sale of firewood from Fungal transmission is
Giberella xylarioides found are produced during the disease intensity dead, infected trees favored by human
(Fusarium xylarioides) rainy season or in moist (45, 53) contributes to the activities in coffee fields
conditions (107) spread of the disease through wounds due to
Microconidia, (45, 53, 107) pruning or weeding
29 June 2018
macroconidia, and (45, 53, 106, 107)

ascospores can be spread
14:15
by water (106, 107)

Root-knot nematodes: Low- to Increase of population No specific information No specific information Competition for

Meloidogyne spp. medium-altitude densities of M. exigua found found resources with
disease for Meloidogyne juveniles in coffee roots Pratylenchus coffeae
exigua: <1,320 MASL during dry periods, sensu lato (4, 54, 55)
in Costa Rica in following root flushes Many hosts within plants
2002–2003 (4) that emerged in previous and weeds of the coffee
wet periods (2, 127) agroecosystem (12, 76)
Increased population
densities in sandy soils
with low levels of
organic matter (4, 54)
and short planting
distances within coffee
rows (4)
Root-lesion nematodes: High-altitude disease: Increase of population No specific information No specific information Wide range of hosts,
Pratylenchus spp. 1,200–1,480 MASL in densities of P. coffeae in found found including weeds (123)
Costa Rica in coffee roots during dry Competition for
2002–2003 (4) periods, following root resources (4, 54, 55)
flushes that emerged in with Meloidogyne spp.
previous wet periods Increased population
(137) densities with short
www.annualreviews.org • Multiple-Disease System in Coffee

planting distances
within coffee rows (4)
27.11
Branch dieback No specific information No specific information Shade regulates fruit No specific information Heavy defoliations due
found found load and decreases the found to coffee leaf rust can
fruit-to-leaf ratio, lead to dieback (36, 81)
avoiding overbearing
dieback (27, 36)
(Continued)
PY56CH27_Avelino
Table 2 (Continued)
ARI
Topography/
27.12
Diseases of secondary importance
Brown eye spot: High temperature Free water is needed for Shade controls the No specific information Increased incidence and
29 June 2018
Cercospora coffeicola requirement (30◦ C) for germination (40), but disease (40, 128), found severity under
Avelino et al.
conidia germination, disease is increased in possibly by regulating conditions of low
14:15
but optimal mycelial plants with hydric stress temperatures and nitrogen supply (28)

growth is obtained at (40) intercepting light that

24◦ C (40, 47) is necessary for
cercosporin
biosynthesis (47)
Phoma leaf blight and High-altitude disease Epidemic development Windbreaks against cold No specific information Injuries (due to insects,
dieback: Phoma (81) during the rainy season winds that cause found wind, friction between
costarricensis Mycelial growth and (39, 81) injuries to leaves and leaves) are necessary
tissue colonization is twigs help to control for infection (39)
improved when disease (81)
temperature range is
17–24◦ C compared to
25–30◦ C; at 30◦ C,
there is no growth or
colonization (39)
Thread blight: No altitude effect Wet conditions needed Shade promotes the No specific information Many hosts, including
Corticium koleroga highlighted (118) (81) disease, probably due to found trees present in coffee
increased wetness (81, agroforestry systems
116); shade regulation (18, 116)
is used for control
purposes (116, 118)
Abbreviation: MASL, meters above sea level.

blight (TB) caused by Corticium koleroga (81, 116), mainly by creating humid conditions within the
plantation (Table 2). However, shade hampers several coffee pathogens: PB by intercepting cold
winds (81) that cause injuries to leaves and twigs, creating entry points for the fungus; BES (40,
128) probably by regulating temperatures and intercepting light necessary for the biosynthesis of
cercosporin, a pathogen toxin (47); and branch dieback by regulating fruit load (27, 36). Fertilizer
applications have also been reported to reduce the incidence of CLR and ALSD, possibly due
to dilution effects (41) in relation to the increased emergence of healthy leaves in well-fertilized
plants, which dilutes the disease. In addition, high planting densities favor CLR (86) and ALSD
(5), probably because leaf wetness is higher and contacts between leaves are improved.
D&P can be associated in injury profiles—that is, a given combination of injury levels caused
by a range of D&P (1, 29, 110–114). This is because D&P are often influenced by similar drivers,
despite influences in different directions, as described in the previous paragraph (Table 2). Injury
profiles (IPs) in coffee have been documented in one detailed study generated by two surveys
conducted in Costa Rica (1) (Figure 4). The main D&P observed in these two surveys were CLR,
BES, ALSD, RKNs, RLNs, and dieback. However, IPs were strongly discriminated according
to rare D&Ps. CLR appeared to be associated with BES, RKNs, and eventually dieback, and
TB; ALSD was associated with RLNs and PB; and LMs were associated with Ceratocystis wilt
Coffee
leaf rust
Ceratocystis (25, 16.4) Brown
wilt 2.5 eye spot
(1.6, 2.2) (24.8, 11.4)
0.0
Leaf miner American leaf

(2.7, 2.1) spot disease
(10.2, 11.9)
IP1 (n = 24)
–2.5 IP2 (n = 44)
IP3 (n = 24)
IP4 (n = 44)
Phoma Root-lesion
leaf blight nematodes
(3.4, 2.9) (1804, 2497)
Thread Root-knot
blight nematodes
(3.7, 5.3) Dieback (31626, 39186)
(9.2, 8.3)
Figure 4
Injury profiles, that is, a given combination of injury levels caused by a range of diseases and pests (1, 29,
110–114), in Costa Rican coffee agroforestry systems. Abbreviations: ALSD, American leaf spot disease;
BES, brown eye spot; CLR, coffee leaf rust; CW, Ceratocystis wilt; DB, dieback; IP, injury profile; LM, leaf
miner; n, number of coffee plots; PB, Phoma leaf blight; RKNs, root-knot nematodes; RLNs, root-lesion
nematodes; TB, thread blight. Data (mean, standard deviation) are standardized to compare injury levels that
have been characterized using different methods and variables. The variables for ALSD, BES, CLR, LM,
and PB are the maximal percentage of young leaves infected in the year; for CW, DB, and TB, the
percentage of coffee plants infected in the plot; for RKNs and RLNs, the number of individuals in 100 g of
coffee roots. Data are from two surveys conducted in Costa Rica (1).

(CW) caused by Ceratocystis fimbriata (Figure 4). IPs have been related to PSs in crop loss studies,
particularly in rice (111, 114, 149), wheat (148), and recently, in coffee (29).
DESIGN AND MANAGEMENT OF COFFEE AGROFORESTRY SYSTEMS

BASED ON CROP LOSS AND ECOSYSTEM SERVICES ASSESSMENTS
Many elements may contribute positively or negatively to the sustainability of (agroecological)
systems (43, 93). In AFSs, the sustainability of agroecosystems is improved by the presence of
trees and the ESs they provide, but trade-offs between services may occur (64, 100). Sustainable
agroecosystems should provide a good balance between ESs to ensure the well-being of a farmer’s
household and also that of other stakeholders, considering the economic value of these services
(96). In this context, multiple D&P management is necessary, since ES provision can be reduced
directly or indirectly by high D&P levels as well as by D&P control methods that have negative
environmental impacts (33). Therefore, the analysis of relationships among ESs is useful for
identifying either trade-offs and the measures needed to avoid them or specific systems that offer
desired levels of several services simultaneously and serve as models to follow (29, 100).
Two steps are proposed for the design of sustainable crop management systems in AFSs. First,
the crop loss assessment of multiple D&P identifies crop health management systems associated
with the lowest losses due to D&P (110, 112). Second, crop loss caused by multiple D&P provides
a quantification of the D&P regulation service in agroecosystems (9, 29), within a larger level
where the value of all ESs is taken into account.
Diversified coffee AFSs have the highest capacity to provide multiple ESs simultaneously, as
demonstrated in a recent study (30) where the relationships between indicators of provisioning
and regulation services were analyzed in coffee monocultures and various coffee AFSs (29, 30).
The most promising coffee AFS plots combined desired characteristics of low crop loss to D&P
(low number of dead productive branches; see below), high yields of coffee and production of other
products (bananas, fruits, timber), sequestered carbon in the aboveground biomass, and good soil
fertility (low soil acidity and adequate contents of macro and micronutrients for the coffee crop).
Furthermore, these promising AFSs had some differences in the complexity of shade canopy and
crop management intensity, which offered a menu of options for the (re)design and management
of coffee agroecosystems (29) to producers according to their objectives and resources. Such an
approach is likely to be useful for other perennial crops.
ASSESSMENT OF YIELD LOSSES DUE TO DISEASES

AND PESTS IN COFFEE
The ability to assess crop losses is required to design sustainable management systems (110, 112).
Crop loss assessment in perennial crops is particularly difficult because D&P may lead to primary
and secondary yield losses (150). Primary yield losses are the consequence of direct effects of
D&P on yield, affecting coffee flowers, fruits, and beans, and of indirect effects, affecting leaves,
wood, and roots (Figure 2). Because coffee berries are borne by the wood produced the previous
year, any injury affecting branch growth also affects subsequent production (Figure 2). In the
only published study on coffee yield losses due to multiple foliar D&P (CLR, BES, anthracnose,
and LM), Cerda and colleagues (29, 31) reported secondary yield losses that were higher than
the primary yield losses (38% compared to 26%, with respect to the attainable yield). This result
is based on an innovative three-year field trial at full sun exposure with different sequences of
pesticide applications. By assessing the production obtained with these different sequences, Cerda
and colleagues (29, 31) came up with estimates for attainable yield and yield losses, individually
27.14 Avelino et al.

(primary loss and secondary loss) and jointly (cumulative loss). In addition, they identified the
number of dead productive branches after the harvest as the best yield-reduction predictor to
explain primary and secondary yield losses due to foliar D&P. Similar results were obtained
through a two-year survey, where crop losses due to D&P were assessed over a range of PSs but
with high variability depending on the plots (29). Primary yield losses varied from 0 to 50% and
resulting economic losses between US$0 and US$2,000 per hectare per year. Secondary yield
losses ranged from 0 to 100% with resulting economic losses ranging from US$0 to US$3,000
per hectare per year. No statistically different yield and economic losses were found among shade
systems (full sun, low diversified AFSs, and highly diversified AFSs). However, the most promising
coffee AFSs showed notably lower losses than the rest of coffee agroecosystems, given that their
primary yield losses were <6% and resulting economic losses less than US$120 USD per hectare
per year, and their secondary yield losses were <18% and resulting economic losses less than
US$600 per hectare per year (29).

CONCEPTS FOR A SYSTEMS APPROACH TO UNDERSTANDING AND

MODELING CROP LOSSES IN THE COFFEE AGROSYSTEM
Yield loss estimates generated from experimental and survey measurements, as described in the
previous section, provide information that is required for crop health analysis. Understanding and
quantification of the effects of D&P on coffee according to the processes involved can also provide
a strong basis for designing improved strategies for D&P management. The interactions between
D&P and the physiology of coffee are dynamic and involve feedbacks in response to a number of
direct and indirect effects. Systems analysis (88, 150) offers a powerful approach for the appraisal
of such interactions. This section is intended to outline current approaches to systems analysis for
coffee health and crop loss assessment.
Damage Mechanisms Associated with Coffee Diseases and Pests

Damage mechanisms refer to the effects of D&P on physiological processes involved in plant
growth and yield buildup (22, 98). In spite of the broad biological and ecological diversity of D&P
that can affect a crop, disease- or pest- triggered damage mechanisms can affect crop physiology
in only a limited number of ways. The main damage mechanisms are as follows (22, 98, 99, 113):
Light stealer: reduces the intercepted radiation—the green leaf area index
Leaf senescence accelerator: increases leaf senescence and causes defoliation
Tissue consumer: reduces the tissue biomass
Stand reducer: reduces the number and biomass of plants
Photosynthesis rate reducer: reduces the rate of carbon uptake
Turgor reducer: disrupts xylem and phloem transport
Assimilate sapper: removes soluble assimilates from host
The above damage mechanisms were defined with annual crops as the main reference. However,
they also apply to perennials, particularly coffee, with limited alterations, because the physiological
processes affected by D&P, such as photosynthesis and transport in vessels, are common in annual
and perennial crops.
Development of a Systems Modeling Structure for the Coffee

Diseases-and-Pests System
Agrophysiological models that include damage mechanisms have been developed for a range of
crops, including wheat (105, 148), rice (14, 92, 149), groundnuts (108), and potatoes (61). The use
of such models provides estimates of yield loss caused by combined as well as individual D&P.
Incorporation of secondary losses is important when considering the effects of D&P on perennials.
The damage mechanisms incurred by D&P may cause a reduced accumulation of reserves, leading
to reduced growth later on, when these reserves would have been remobilized. For example,
grapevine rust causes defoliation after harvest, which reduces the allocation of photosynthates to
reserves between harvest and leaf fall, and further impairs growth when the next crop cycle starts
at the end of winter (94). CLR also reduces the storage of reserves through intense sporulation and
by causing defoliation. However, since CLR preferentially affects high-yielding trees, its effect is
exacerbated by the fruits’ high demand for carbohydrates, which can cause a depletion of reserves
in the wood and reduced growth of the coffee tree, leading to diebacks, even in the absence of leaf
diseases (27, 36).
Modeling of yield losses in perennials using a process-based approach has been limited and has
mainly considered individual diseases or pests. Recent studies have accounted for the polyetic effect
(150) of aphid infestation on peaches (20). Agrophysiological models for coffee have been recently
developed to analyze the performance of coffee in AFSs (134), to simulate coffee production and
phenology (103), and to simulate the CBB dynamics according to the number of berries available
for attack (104).
We propose here a systems-, process-based approach and a model structure where the effects
of D&P on coffee production are explicitly considered, including physiological processes that
can be affected by D&P and processes associated with the buildup of secondary losses (polyetic
physiological processes). In view of the previously described damage mechanisms associated with
D&P, we propose a model structure that fulfills the above criteria, as described in Figure 2. This
modeling structure is derived from GENECROP, a generic agrophysiological model for yield
loss analysis. The structure of GENECROP was designed for annual crops (148, 149). Additional
processes important for perennial crops (reserve dynamics) have been incorporated in the structure
proposed for a perennial crop such as coffee.
The model structure considers a series of state variables that are the biomasses of the different
plant organs: the roots (BRoot), leaves (BLeaf ), fruits (BFruit), stems (BStem), and wood and trunk
(BWood&Trunk). These state variables all have biomass, [M], as a dimension. Stems are defined
as annual shoots produced within the crop cycle. Stems become wood at the end of the crop
cycle.
As in GENECROP, the model includes the main processes involved in crop growth
(Figure 5):
RPhot, the rate of photosynthesis
RPart, the rate of partitioning of carbohydrates toward organs
RSenL, the rate of physiological leaf senescence
Additional processes for perennial crops are incorporated in the model, allowing the consider-
ation of successive crop cycles (Figure 5). The rates (all with dimension [M/T]) associated with
these processes are as follows:
Accumulation of reserves from roots (RReservesRoot), stems (RReservesStem), and wood and
trunk (RReservesW &T)
Remobilization of reserve carbohydrates (RReservesUse)
Transfer of stem biomass to wood at the end of the growth cycle (RTRA; stems become
wood)
Pruning included as outflows from leaf and stem biomass (RPruL and RPruS)
Damage mechanisms for D&P can be included in this generic model structure for perennial crop
growth (Figure 5):

Turgor
reducer
RAD
Photosynthetic
rate reducer
Light stealer RUE
Assimilate RPhot
sapper k
LA
RUptake RReservesUse
Carbo
RPartWood&Trunk
Stand reducer
RPartLeaf RPartStem BWood

&Trunk
RPartRoot RdeathWT
RPartFruit RdeathSt
BWood
BLeaf BFruit BRoot BStem &Trunk
RTRA
RPruS
RPruL RconsF RReservesStem

RSenL
RHarvest
Leaf senescence RReservesW&T

accelerator
Reserves
Harvest Tissue RReservesRoot
Turgor consumer
reducer
Figure 5
A flowchart for a process-based, mechanistic simulation of coffee growth affected by multiple diseases and pests, including damage
mechanisms. (Blue) Agrophysiological processes and variables for annual and perennial crops: photosynthesis (RPhot), radiation (RAD),
radiation use efficiency (RUE), leaf area (LA), partitioning of the carbohydrates toward the different plant organs (RPart), and leaf
senescence (RSenL). (Brown) Processes and variables for perennial crops: accumulation of reserves from roots (RReservesRoot), stems
(RReservesStem), and wood and trunk (RReservesW&T); remobilization of reserve carbohydrates (RReservesUse); rate of transfer of stem
biomass to wood at the end of the growth cycle (RTRA) (i.e., stems become wood); and pruning of leaf (RPruL) and stem (RPruS)
biomass. (Red) Processes and variables for damage mechanisms: light stealers (e.g., coffee leaf rust, American leaf spot disease, brown
eye spot) reduce the green leaf area; the effects of assimilate sappers (coffee leaf rust) translate into an outflow from the pool of
carbohydrates (RUptake); tissue consumers (coffee berry borer) decrease the fruit biomass (RconsF); leaf senescence accelerators (coffee
leaf rust, American leaf spot) reduce the amount of leaf biomass (RSenL); stand reducers (dieback) reduce the biomass of wood and stem
through an outflow from these state variables (RDeathWT, RDeathSt); photosynthesis rate reducers (brown eye spot) reduce the RUE;
and the effects of turgor reducers (root-knot nematodes, root-lesion nematodes) translate into reduced RUE and accelerated leaf
senescence (RSenL).

Light stealers (for instance, CLR, ALSD, and BES) reduce the green leaf area.
Assimilate sappers (CLR) effects translate into an outflow from the pool of carbohydrates
(RUptake).
Tissue consumers (CBB) decrease the fruit biomass (RconsF ).
Leaf senescence accelerators (CLR, ALSD) reduce the amount of leaf biomass (RSenL).
Stand reducers (dieback) reduce the biomass of wood and stem through an outflow from
these state variables (RDeathWT and RDeathSt).
Photosynthesis rate reducers (BES) reduce the RUE (radiation use efficiency).
The effect of turgor reducers (RKNs) translates into a reduction in RUE and an acceleration
of leaf senescence (RSenL).
This system model can be used to explore the effects of multiple D&P on growth and yield of
coffee over successive crop cycles. This modeling structure could also be used to address other
perennial crops.
CONCLUSION
Crop loss assessment provides key information for the development of sustainable crop manage-
ment systems. Leverage points for crop health management can be identified by understanding
the conditions leading to D&P development and the resulting crop losses. Crop loss assessment is
also useful for the evaluation of the D&P regulation service, which is a necessary step toward the
design of sustainable crop management systems where the provision of ESs is optimized, taking
into account possible trade-offs between services.
As demonstrated in this review, crop loss assessment is a difficult task particularly in perennial
crops where losses can be delayed over several years and where polyetic effects are common.
Another difficulty is the integration of the multiple-disease system, where each pathogen or pest
has its own damage pathway, depending on the affected organ and the impacts on it. The multiple-
disease system in coffee provides a complex model of a tropical perennial crop, where original crop
loss assessment approaches have been implemented through experiments, surveys, and modeling,
and have been used for the design of crop management systems.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
The authors wish to thank Régis Babin, Fabrice Pinard, Fabienne Ribeyre, and Luc Villain for
critically reviewing the section about the main Arabica coffee D&P and Ree Sheck for reviewing the
English. This review has been made possible thanks to the Mesoamerican Scientific Partnership
Platform: Agroforestry Systems with Perennial Crops (PCP).
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PY56CH27_Avelino ARI 29 June 2018 14:15

Annual Review of Phytopathology

Jacques Avelino,1,2,3 Clémentine Allinne,2,4

Annu. Rev. Phytopathol. 2018. 56:27.1–27.25 Keywords

COFFEE-BASED AGROFORESTRY SYSTEMS AND THE ECOSYSTEM

Complexity of structure and composition

Monoculture Association with other trees Close to natural ecosystems

www.annualreviews.org • Multiple-Disease System in Coffee 27.3

MAIN DISEASES AND PESTS OF ARABICA COFFEE

27.4 Avelino et al.

Root Bean weight

Injuries physiological impacts

b Dieback Primary yield losses

Number of fruiting nodes

Root Bean weight

Number of fruiting nodes

Root Bean weight

www.annualreviews.org • Multiple-Disease System in Coffee 27.5

Hypothenemus hampei pathogen: Mycena Colletotrichum kahawae 135, 143,

Abbreviation: NA, not available.

27.6 Avelino et al.

www.annualreviews.org • Multiple-Disease System in Coffee 27.7

PRODUCTION SITUATIONS IN COFFEE

EPIDEMIOLOGY OF COFFEE DISEASES

27.8 Avelino et al.

Plot biophysical characteristics

Plot biophysical characteristics

www.annualreviews.org • Multiple-Disease System in Coffee 27.9

Table 2 Main drivers of Arabica coffee diseases on susceptible coffee trees

Diseases of primary importance

21–28◦ C (142) infection, but

occur before final publication.)

July 11, 2018. (Changes may still

macroconidia, and (45, 53, 106, 107)

by water (106, 107)

occur before final publication.)

July 11, 2018. (Changes may still

www.annualreviews.org • Multiple-Disease System in Coffee

occur before final publication.)

July 11, 2018. (Changes may still

Abbreviation: MASL, meters above sea level.

Leaf miner American leaf

www.annualreviews.org • Multiple-Disease System in Coffee 27.13

DESIGN AND MANAGEMENT OF COFFEE AGROFORESTRY SYSTEMS

ASSESSMENT OF YIELD LOSSES DUE TO DISEASES

27.14 Avelino et al.

US$600 per hectare per year (29).

CONCEPTS FOR A SYSTEMS APPROACH TO UNDERSTANDING AND

Damage Mechanisms Associated with Coffee Diseases and Pests

Development of a Systems Modeling Structure for the Coffee

27.16 Avelino et al.

Light stealer RUE

RPartLeaf RPartStem BWood

RPruL RconsF RReservesStem

Leaf senescence RReservesW&T

www.annualreviews.org • Multiple-Disease System in Coffee 27.17

27.18 Avelino et al.

www.annualreviews.org • Multiple-Disease System in Coffee 27.19

27.20 Avelino et al.

tional and organic coffee systems in Nicaragua. Nematropica 41:82–90

www.annualreviews.org • Multiple-Disease System in Coffee 27.21

27.22 Avelino et al.

Growth and development of the coffee plant. Ecol. Model. 222:3626–39

www.annualreviews.org • Multiple-Disease System in Coffee 27.23