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Patterns and drivers of fungal disease community on Arabica coffee

along a management gradient

B. Zewdie , A.J.M. Tack , G. Adugna , S. Nemomissa ,

K. Hylander

PII: S1439-1791(20)30055-4
DOI: https://doi.org/10.1016/j.baae.2020.05.002
Reference: BAAE 51259

To appear in: Basic and Applied Ecology

Received date: 3 July 2019

Accepted date: 4 May 2020

Please cite this article as: B. Zewdie , A.J.M. Tack , G. Adugna , S. Nemomissa , K. Hylander , Pat-
terns and drivers of fungal disease community on Arabica coffee along a management gradient, Basic
and Applied Ecology (2020), doi: https://doi.org/10.1016/j.baae.2020.05.002

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Patterns and drivers of fungal disease community on Arabica

coffee along a management gradient

B. Zewdiea,*, A. J. M. Tacka, G. Adugnab, S. Nemomissac and K. Hylandera

a
Department of Ecology, Environment and Plant Sciences, Stockholm University, SE-106 91

Stockholm, Sweden
b
Department of Horticulture and Plant Sciences, Jimma University College of Agriculture

and Veterinary Medicine, P.O. Box 307, Jimma, Ethiopia

c
Department of Plant Biology and Biodiversity Management, Addis Ababa University,

College of Natural Sciences, P.O. Box 3434, Addis Ababa, Ethiopia

*
Corresponding author. Tel.: +46728365337.
E-mail address: beyene.hailu@su.se.

1
Abstract

Plants, including those managed by humans, are often attacked by multiple diseases. Yet,

most studies focus on single diseases, even if the disease dynamics of multiple species is more

interesting from a farmers’ perspective. Moreover, most studies are from single management

systems, although it is valuable to understand how diseases are distributed across broad

management gradients, especially in cases where less intensive management also provides

biodiversity values in the landscape. To understand the spatial dynamics and drivers of

diseases across such a broad management gradient, we assessed the four major fungal

diseases on Arabica coffee (Coffea arabica) at 60 sites in southwestern Ethiopia along a

gradient from only little managed wild coffee in the forest understory to intensively managed

coffee plantations. We found that environmental and management factors related to disease

incidence and severity differed strongly among the four fungal diseases. Coffee leaf rust

(Hemileia vastatrix) and Armillaria root rot (Armillaria mellea) were more severe in

intensively managed sites, whereas coffee berry disease (Colletotrichum kahawae) and wilt

disease (Gibberella xylarioides) were more severe in less managed sites. Among sites,

incidence and severity of the four fungal diseases poorly correlated with each other. Within

sites, however, shrubs that were severely attacked by coffee leaf rust also had high levels of

berry disease symptoms. A better understanding of disease dynamics is important for

providing management recommendations that benefit smallholder farmers, but also to

evaluate possibilities for maintaining biodiversity values in the landscape related to shade

cover complexity and wild coffee genetic variation.

Keywords: coffee, coffee fungal diseases, co-occurrence, disease community, management

gradient, southwestern Ethiopia

2
Introduction

While plants are frequently attacked by multiple diseases, the majority of studies on the

spatial and temporal dynamics and drivers of diseases in natural and agricultural systems have

focused on the disease dynamics of single species (Avelino et al., 2006; Tack, Thrall, Barrett,

Burdon, & Laine, 2012). Hence, we lack insights into the distribution and dynamics of disease

communities: whether diseases attacking the same host plant respond to similar abiotic and

biotic drivers or not and if they are co-distributed. Moreover, the majority of studies on

disease systems have focused on either natural or agricultural diseases, and the link between

disease dynamics in natural and agricultural systems is less investigated. A promising location

to study this link is the plant’s area of origin, where the diseases occur natively on wild plants

as well as on the managed crop. As a way forward, we need to study multiple diseases

occurring on the same host plant across a management gradient spanning from natural to

agricultural systems.

Given the dominance of studies focusing on single plant diseases (Bolton, James

A, & David F, 2008; Marçais & Desprez-Loustau, 2014), our understanding of disease

community dynamics is pieced together from disparate studies on single diseases on the same

or different host plants in different areas across the world. Such single species studies do not

give insights into disease co-occurrence patterns, the degree to which diseases respond to the

same drivers, and the additive or synergistic effects of single versus multiple attacks on plant

fitness. As one example of a study on multiple diseases in a natural community, Desprez-

Loustau et al. (2018) studied the distribution of three cryptic powdery mildew species on oak,

and found that the species strongly differed in their distribution, drivers and co-occurrence

patterns across spatial scales ranging from a single leaf to the continent.

Furthermore, studies of plant disease have generally focused on the dynamics of

diseases either in their natural environments (Ekholm, Roslin, Pulkkinen, & Tack, 2017;

3
Jousimo et al., 2014) or in human-altered agroecosystems (Avelino et al., 2007; Bedimo et al.,

2008). A few studies focus on variation in disease dynamics along gradients of landscape

complexity (Kebede, Baudron, Bianchi, & Tittonell, 2018; Soto-Pinto, Perfecto, & Caballero-

Nieto, 2002), but studies of diseases on crops where the plant is both cultivated and growing

wild in the same landscape are lacking. Yet disease dynamics are likely to vary along such

gradients, for example due to the fact that host and parasites can freely co-evolve in natural

systems, whereas evolutionary changes in agricultural systems are driven by human-imposed

artificial selection (Chen, Gols, & Benrey, 2015).

Arabica coffee (Coffea arabica L.) is grown in a large diversity of management

systems across the tropical world (Moguel & Toledo, 1999; Perfecto, Rice, Greenberg, & Van

der Voort, 1996) and is, as most crops, attacked by a large diversity of diseases and insect

pests (Avelino, Allinne, Cerda, Willocquet, & Savary, 2018). It mainly originates from

southwestern Ethiopia, where more or less wild populations with high genetic diversity are

still present in larger forest tracts (Anthony et al., 2002; Tesfaye, Govers, Bekele, & Borsch,

2014). In southwest Ethiopia, the density and diversity of shade trees vary strongly across the

landscapes: in the most intensively managed sites, coffee is grown under a sparse canopy

layer made up of one or few tree species, while at the natural end of the gradient coffee

berries are harvested from naturally established shrubs under a more or less intact canopy of

the montane forest (Gole, Borsch, Denich, & Teketay, 2008). Of major concern in Ethiopian

coffee systems are several fungal diseases (Hindorf & Omondi, 2011) which often can be

found together in the same sites or on the same coffee plant.

Here, we studied the distribution and co-occurrence patterns of four major

fungal diseases (coffee leaf rust, coffee berry disease, coffee wilt disease and Armillaria root

rot) in 60 Arabica coffee sites in southwestern Ethiopia along a broad management gradient.

More specifically, we addressed the following questions:

4
 (i) To what extent do fungal diseases vary in their incidence and severity within and

among sites?

(ii) What are the impacts of the abiotic and biotic environment and management

intensity on the incidence and severity of the major fungal diseases?

(iii) What is the pattern of co-occurrence of the fungal diseases along the management

gradient?

Materials and methods

Study system

This study was conducted in Gomma and Gera districts of Jimma Zone, southwestern

Ethiopia (7°37’ - 7°56’ N and 36°13’ - 36°39’ E , Fig. 1A and B). The altitude of the study

area ranges from 1500 to 2100 m a.s.l. The area receives an annual rainfall in the range of

1480 to 2150 mm, with the main rainy season between June and September, and has mean

daily minimum and maximum temperatures of 12 °C and 28 °C, respectively. The study area

has a mosaic landscape with tree-covered areas such as forests and shade coffee plantations

but also open areas for annual agriculture (Lemessa, Hylander, & Hambäck, 2013). The

climax vegetation in this region is moist Afromontane forest with mostly evergreen trees such

as Syzygium guineense, Schefflera abyssinica, Prunus africana, Pouteria adolfi-friederici,

Ficus sur and Olea welwitschii (Friis, Sebsebe, & Breugel, 2010). Coffee is the main source

of cash income for the population in the study landscape (Ango, Börjeson, Senbeta, &

Hylander, 2014; Dorresteijn et al., 2017) and is grown across the whole landscape under

various management intensities. We note that some authors use a terminology in which the

coffee growing systems of southwestern Ethiopia are divided into several categories

depending on management intensity, i.e. forest coffee, semi-forest coffee, semi-plantation

coffee and plantation coffee (Aerts et al., 2011; Hundera et al., 2013). However, our plots are

5
selected from a landscape with a clear continuous gradient in attributes such as coffee

structure and tree layer composition, and we therefore chose to regard management intensity

as a continuous gradient. Coffee generally originates from the natural gene pool and farmer’s

landraces or, in a few cases, especially in plantations of private companies, cultivars that are

resistant to coffee berry disease. At smallholder level, coffee production in the area is

generally organic, while fertilization and use of herbicides is a common practice in the

plantations. The main fungal diseases on coffee are: coffee leaf rust (Fig. 2A) caused by

Hemileia vastatrix that leads to defoliation, the coffee berry disease (Fig. 2B) caused by

Colletotrichum kahawae that mummifies immature coffee berries, coffee wilt disease (Fig.

2C) caused by Gibberella xylarioides and root rot (Fig. 2D) caused by Armillaria mellea that

kill infected coffee shrubs (see Appendix A for details of the diseases). To our knowledge

neither fungicides nor insecticides are applied to control diseases or pests in any of the coffee

systems in southwestern Ethiopia.

Study design

Based on Google Earth pictures and short field visits, we selected 60 sites varying in tree

cover complexity (e.g. canopy cover, vertical layers and species richness) and coffee

management intensity across the focal landscape (Fig. 1A and B), while aiming to avoid

spatial autocorrelation in these variables. In each site we established a plot of 50 × 50 m and

marked 16 coffee shrubs on intersections of the 10 × 10 m quadrants in the central 30 × 30 m

area (Fig. 1C).

Assessment of fungal diseases of coffee

We assessed coffee leaf rust from 3 March to 5 May 2017 taking care to visit different parts

of the landscape each day (to avoid biases due to date). Three bearing branches per shrub

6
(from the base, middle and upper part) were selected and assessed for presence/absence of

rust pustules/lesions (≥20 leaves per branch). Newly unfolding leaves on the two nodes at the

tip of the shoots were not considered for leaf rust assessment as they are less susceptible

(Chala, Chemeda, Girma, & Holger, 2010). If no leaves on the selected branches had coffee

leaf rust infection, we searched an additional c. 2 min for the presence of infection on the

remaining part of the coffee shrub. Coffee berry disease, coffee wilt disease and Armillaria

root rot were assessed from 19 July to 26 August 2017. Number of bearing branches with

coffee berry disease symptom and proportion of berries infected with coffee berry disease

were recorded for each of the 16 coffee shrubs per site. The number of coffee shrubs with

coffee wilt disease and Armillaria root rot symptoms were counted within the 50 × 50 m plot.

The rust is more severe during the dry season compared to the wet season, motivating the

different surveying periods (See also Appendix A). We here define incidence as the

proportion of infected out of the total number of coffee shrubs per site (for coffee wilt disease

and Armillaria root rot) and severity as proportion of leaves/berries infected out of the total

number of leaves/berries assessed (for coffee leaf rust/coffee berry disease).

Environmental variables

To assess canopy cover, we took five pictures of the shade tree canopy above coffee height

(by elevating the camera with a stick) in the central 30 × 30 m plot from the central and

corner quadrants (see Fig. 1C). The pictures were subsequently analyzed using ImageJ

software, version 1.50i (Schneider, Rasband, & Eliceiri, 2012). Slope of the plot was

measured with a clinometer (Suunto Clinometer PM5/360). Density of coffee and non-coffee

shrubs was counted in the 30 × 30 m plot. Shade trees with diameter at breast height (DBH)

>20 cm were identified and counted in the 50 × 50 m plot. Tree cover in an area of 1 km

buffer surrounding each of the 60 sites was measured using ArcMAP (Version 10.6.1) from

7
ArcGIS Desktop from a manually interpreted map of forest polygons. We developed an index

based on the typical growth pattern of coffee under different types of management to describe

the gradient in management intensity across the sites (see Appendix B). This site level index

ranges from 1 (only little managed coffee, often in the natural forest) to 3 (heavily pruned

coffee, often in plantations), and will henceforth be referred to as ‘coffee structure index’. We

also developed an index involving the main coffee management activities (pruning, nutrition

and weeding) to get an impression of how coffee management relates to the different diseases

(see Appendix B).

Statistical analyses

To understand the variation in disease dynamics among sites we fitted generalized linear

(mixed) models with several predictor variables. For proportion data (coffee leaf rust,

branches and berries infected with coffee berry disease, all assessed at the level of individual

coffee shrubs), a generalized linear mixed model (GLMM) with binomial distribution was

fitted using the lme4 package (Bates, Mächler, Bolker, & Walker, 2014). Nine predictor

variables (see below) were used as fixed factors. To account for correlation among individual

trees within a site, we included the random factor ‘site’. The proportion of coffee shrubs with

coffee wilt disease and Armillaria root rot (both assessed at site level) were modelled using a

generalized linear model (GLM) with binomial distribution. Partitioning of variance in

disease frequencies within and among sites was performed for the fungal diseases surveyed at

coffee shrub level using the lme4 package (GLMM). We adopt the approach of McMahon and

Diez (2007) to assume that the level 1 random effect (within-site variation) is logistically

distributed with mean zero and variance π2/3. The proportions of within-site and among site

variation was calculated as π2/3/( π2/3 + τβ) and τβ/(π2/3 + τβ) respectively, where τβ is the

8
level 2 random effect variance retrieved from the fitted models. For all the statistical analyses,

we used the statistical software R version 3.5.1 (R Core Team, 2018).

To account for variation along the gradient (e.g. resource concentration, light

intensity, microclimate, natural complexity among sites), eight environmental and stand

structure variables measured at the site level (altitude, slope, coffee density, proportion of

non-coffee shrubs to coffee, canopy cover, shade trees >20 cm DBH, surrounding tree cover,

coffee structure index and management index) were proposed to be included in the models.

However, prior to the final statistical analysis, we assessed the correlation among the

predictor variables and decided to omit management index due to the strong correlation with

coffee structure index (see Appendix C: Table C1). We scaled all predictor variables to zero

mean and unit variance. Additionally, for coffee leaf rust and berry disease, the sampling date

was included as a covariate to account for temporal variation in disease incidence and

severity. The models were simplified by repeatedly dropping the predictor variable explaining

the least variation in the response variable, using a cut-off p-value of 0.05 (Crawley, 2012).

To validate that the absence of an effect of an explanatory variable was not due to co-

variation with other explanatory variables, we also ran separate regression models for each of

the dropped variables.

To analyze the relationship between the different fungal diseases, we first ran

Pearson correlation tests to see if the severity of the different diseases co-varied among sites.

As a second step, and because environmental variables may obscure the relationship between

the different diseases, we also checked correlations of the residuals extracted from the full

models explained in the previous paragraph. Finally, for diseases assessed at the individual

coffee shrub level (leaf rust and coffee berry disease), we fitted a generalized linear mixed

effects model (GLMM) with one of the diseases as response variable and the other as a

9
covariate, and site as a random effect, to test for the within site co-variation between the two

species.

Results

Variation in the environmental factors and disease levels within and among sites

Environmental and stand structure variables varied strongly among the sixty sites (Table 1).

For example, shade canopy cover ranged from 13 to 83% and the number of larger shade trees

ranged from 5 to 43 tree individuals (Table 1). Coffee density was generally high, and it was

the dominant shrub along the entire gradient (Table 1).

The fungal diseases differed strongly in their site-level prevalence: coffee leaf

rust and coffee wilt disease occurred in all or nearly all sites (60 and 57 out of the sixty sites,

respectively), coffee berry disease was found in the majority of sites (46), and Armillaria root

rot was present in half of the sites. The severity of coffee leaf rust was highly variable among

sites (ranging from 0.1 to 35% of infected leaves), but even more variable among shrubs

within sites (Table 2). In contrast, infection of berries by coffee berry disease was more

variable among sites than among shrubs within sites (Table 2). While coffee wilt disease and

Armillaria root rot were both present in a large fraction of our sites, their incidence within

sites was relatively low, with a maximum of 5% of infected coffee shrubs per site (Table 2).

The relationship between environment, management intensity and severity of fungal diseases

Coffee leaf rust severity decreased with altitude and canopy cover (Table 3, Fig. 3A and B),

with the effect of canopy cover only significant in the separate regression model (Table 3).

Moreover, coffee leaf rust severity decreased during the survey period, but increased with the

surrounding forest area within a 1-km buffer (Table 3). In contrast to the coffee leaf rust, the

proportion of branches infected with coffee berry disease, as well as the proportion of infected

10
berries, increased with altitude (Table 3, Figs 3D and C1). Coffee berry disease was more

pronounced on trees with a lower value of coffee structure index, which is characteristic for

sites with less intensive management (Table 3, Figs 3F and C1).

Coffee wilt disease was affected by several environmental variables (Table 3): the

incidence increased with shade canopy cover (Fig. 3H) and number of large shade trees

(Table 3), but decreased with coffee density (Table 3). There was a weak positive relationship

with altitude, even though this relationship was only significant in the separate regression

model (Table 3, Fig. 3G). The incidence of Armillaria root rot increased with altitude, shade

canopy cover, coffee structure index, and number of large shade trees (Table 3, Fig. 3J-L).

The disease incidence decreased with coffee density (Table 3).

Co-occurrence patterns of the major fungal diseases

Pearson correlation analyses of the relationship between the different fungal diseases

indicated that the four fungal diseases did not co-vary across sites, as evidenced by the weak

and non-significant pairwise correlations (r< |0.22|, p > 0.085, see Appendix C: Table C2).

Similarly, the correlations between the residual values extracted from the disease models

reported in the previous section, which reflect the variation in disease levels remaining after

accounting for the environmental and management variables, were all non-significant (r<

|0.12|, p > 0.34, see Appendix C: Table C3). However, coffee leaf rust and berry disease co-

occurred more frequently on the same shrubs within sites (SC = 0.27, χ2 = 133.9, p < 0.001,

see Appendix C: Table C4, Fig. C2).

Discussion

We studied a fungal disease community on Arabica coffee along a management gradient from

only little managed wild coffee under a natural forest canopy to intensively managed

11
plantations, within the crop’s native range. All four diseases had high incidence across the 60

investigated sites. However, the incidence and severity of each disease was related to different

combinations of environmental (like altitude and shade cover) and management variables

along the gradient and did not co-occur more or less often than chance at the same sites.

However, within sites, shrubs with a higher severity of coffee leaf rust also had more coffee

berry disease and vice versa even if this pattern was weak. Overall, our findings indicate that

altitude, canopy cover and management intensity are crucial in driving disease distributions,

but that fungal species differ in the direction and strength of their response to these

environmental factors.

Variation in disease levels within and among sites

Pathogen species showed strongly divergent multi-scale distributional patterns, despite being

present within the same landscape and attacking the same host plant. Coffee leaf rust severity

was highly variable among sites, but even more so among shrubs within sites. The large

within-site variation in coffee leaf rust may be due to a high sensitivity to the local

microclimate (Samnegård, Hambäck, Nemomissa, & Hylander, 2014). For example, small-

scale heterogeneity in canopy cover is common, and may affect both the microclimate and

splash dispersal (Avelino, Willocquet, & Savary, 2004). Coffee shrubs close to infected

shrubs could also be at a higher risk of receiving spores dispersed by rain, wind and coffee

pickers (Waller, 1982), thus creating a within-site spatial clustering.

In contrast to leaf rust, coffee berry disease varied more among sites than among

shrubs within sites. One reason may be that coffee berry disease responds to environmental

factors that are less heterogeneous at the small scale (Derso & Waller, 2003), or that efficient

within-site dispersal results in more uniform infection levels within sites. Importantly,

resistance against this disease is present within wild coffee populations. Besides, locally-

12
selected varieties with resistance against coffee berry disease have been released by Jimma

Agricultural Research Center (JARC). Hence, among-site variation may be either a natural

phenomenon, or due to some farmers using cultivars that differ in resistance to the coffee

berry disease. A promising future avenue for research is to interview farmers about the origin

of their coffee plants, as well as characterization of neutral and adaptive genetic variation

among and within sites. The latter approach may also identify valuable genetic material for

breeding purposes.

The drivers of a disease community on coffee

When focusing on a disease community on Arabica coffee, we found that the strength and

direction of the effect of environmental drivers and management differed strikingly among the

individual diseases. In general coffee leaf rust and Armillaria root rot were more common in

intensively managed sites, while coffee berry and coffee wilt diseases were more common in

the less intensively managed part of the gradient. As a proxy for climate, altitude seemed to

be an important driver, but in different directions. Our findings that altitude negatively

correlated with coffee leaf rust severity, but positively affected coffee berry disease levels

confirm previous studies on coffee leaf rust (Chala et al., 2010) and coffee berry disease

(Hindorf & Omondi, 2011). Coffee leaf rust was also more severe under lower shade canopy

cover (see also Soto-Pinto et al., 2002). As more open canopies create a warmer temperature

and lower humidity, the climatic drivers behind the effect of shade canopy cover may then be

similar to those that shape the altitudinal disease gradient. However, under laboratory

conditions, coffee leaf rust requires high air humidity or moisture on the leaf surface to

germinate and a temperature in the range of 22-28 °C to cause infection and sporulation

(Nutman, Roberts, & Clarke, 1963; Waller, 1982). Hence, we tentatively suggest that

moisture levels are high enough for the rust to thrive in the low altitude and low canopy cover

13
sites investigated by us (c.f. López-Bravo, Virginio-Filho, & Avelino, 2012), whereas

temperature could be the limiting factor at higher altitudes. Dispersal from surrounding areas

might play a role for local levels of coffee leaf rust, since there was somewhat higher severity

in sites with more tree-cover in the surrounding 1-km buffer.

In our study, both coffee wilt disease and Armillaria root rot increased with

altitude and canopy cover, but had higher disease levels at opposite ends of the management

gradient, with coffee wilt disease more common in the less managed forest sites and

Armillaria root rot more common in intensively managed sites. The affinity of coffee wilt

disease to higher altitudes was surprising since it has been known to occur over a wide

altitudinal range and has previously been reported as a major problem in lowland areas of

coffee production in Ethiopia (Girma, Hulluka, & Hindorf, 2001). The spread of Armillaria

root rot among neighboring shrubs is facilitated by its rhizomorphs that prefer cooler

environments to develop (Gezahgne, Coetzee, Wingfield, Wingfield, & Roux, 2004; Otieno,

Sierra, & Termorshuizen, 2003) and this may explain the higher frequency of infection at

higher altitudes.

Co-occurrence among pathogen species

Species may co-occur if they respond to the same environmental variables, i.e., if local

conditions fall within the fundamental niche of both species (Chunco, Jobe, & Pfennig, 2012).

Since all the four diseases we investigated changed in severity along the altitudinal gradient

(positive or negative) it could be expected that they would have shown significant co-

occurrence patterns across sites (either positive or negative). However, this was not the case

implying that the diseases have individual responses in relation to several other drivers, even

if they were all partly driven by altitude.

14
 However, our findings indicate that, within a site, shrubs with severe leaf rust

infection also had a higher proportion of berries infected by coffee berry disease (and vice

versa). Even if this pattern was rather weak, it is suggesting that there could be a direct or an

indirect interaction between the two diseases. One possible mechanism accounting for this

pattern could be that an infected and subsequently weakened host is more susceptible to

infection by another pathogen (Singer, 2010). Interestingly, a very similar case was reported

from Costa Rica where coffee leaf rust and the American leaf spot disease (caused by Mycena

citricolor) were inversely driven by altitude, but still had a positive association (Allinne,

Savary, & Avelino, 2016; Avelino et al., 2018).

Implications for management

Since the four diseases were characterized by their own niches and different, sometimes

contrasting relationships with the environment, it is inherently difficult to come up with

simple management recommendations for the whole disease community (see Jonsson,

Raphael, Ekbom, Kyamanywa, & Karungi, 2015). Even coffee berry disease, coffee wilt

disease and Armillaria root rot, which all increased in prevalence at higher altitudes, did not

positively co-vary among the sites, showing that the combination of conditions that favor one

species might not favor another. This is an important take home message from this study,

which would not have been possible by a series of separate studies focusing each on a single

disease.

However, based on our field observations and discussions with farmers, coffee

berry disease is perhaps the most problematic in terms of its effect on the harvestable yield

and might thus be the species to focus most on (see also Alemu, Adugna, Lemessa, & Muleta,

2016; Garedew, Lemessa, & Pinard, 2017). On the other hand, coffee wilt disease and

Armillaria root rot kill all infected coffee shrubs and therefore cause considerable yield

15
losses. Also, the higher occurrence of coffee wilt disease in less managed forests warrants

consideration since it could endanger the in situ conservation of the genetic diversity of coffee

(Getachew, Adugna, Lemessa, & Hindorf, 2012, 2013). Yet, even if coffee leaf rust is not

regarded as a major problem by local farmers (personal communication), this may be an

underestimation as the infection symptoms are not related to a direct yield loss (Hindorf &

Omondi, 2011).

In southwestern Ethiopia, smallholder coffee production usually follows the

‘low input – low output’ principle (Petit, 2007). At the same time, the farmers’ goals are to

increase yield, receive a better revenue at lower costs of production, and stabilize yield among

years. Thus, from the farmer’s perspective it is the combined effect of diseases and pests in

combination with the amount of invested labor that will matter in the end. However, it is also

important to note that shaded coffee systems have other values for the society than direct

revenue from berry production. They harbor high biodiversity both at a local scale (Buechley

et al., 2015; Schmitt, Senbeta, Denich, Preisinger, & Boehmer, 2010; Tscharntke et al., 2015)

and as part of the landscape (Hylander & Nemomissa, 2008; Shumi et al., 2018; Tscharntke,

Klein, Kruess, Steffan‐Dewenter, & Thies, 2005). Yet, another biodiversity value with these

landscapes is the genetic pool of wild coffee. Thus, attempting to approach coffee berry

disease problems with resistant coffee genotypes should be done cautiously, since it could

ruin the genetic diversity of coffee in its native forests (see Aerts et al., 2013). Future research

thus needs to assess to what extent yield and farmers’ revenues trade-off against biodiversity

values in this system and if management to reduce the impact of different fungal diseases can

modify such relationships. Given these complexities there is much to win by developing

nature-based solutions to disease problems, but local farmers might need financial support, for

example through certification programs (Gove, Hylander, Nemomisa, & Shimelis, 2008;

Tscharntke et al., 2015).

16
Acknowledgement

This work was supported by a grant from the Swedish International Development Agency

(Grant no. VR2015-03600 to KH). We would like to thank coffee owners for allowing us to

work in their coffee plots, the local and regional administrations for providing the permits to

work in the coffee forests, Irena Koelemeijer for providing us with the landscape data and

Tijani Ibrahim for his assistance during data collection.

Declaration of interest

Authors declare no conflict of interest.

Appendices A-C. Supplementary data

Supplementary data associated with this article can be found, in the online version, at

XXXXX.

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25
Figures

Fig. 1. Study area and plot design. Panel (A) shows a map of Ethiopia, with the study area in

southwestern Ethiopia indicated by a red rectangle. Panel (B) shows an aerial view of the

study landscape, where the black dots represent the sixty sites established within the

landscape. The landscape is characterized by tree-covered forest areas (dark green) and open

areas for annual agriculture (light green). Panel (C) shows the layout of the individual plots.

26
Each plot is 50 × 50 m, with the sixteen focal coffee trees selected at the intersection of 10 m

grid-lines within the core 30 × 30 m of the plot (the area marked in grey). Each of the focal

coffee shrubs was labelled with a metal tag and forest spray. Shade canopy pictures were

taken from five locations, as indicated by the blue dots.

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Fig. 2. Major fungal diseases of coffee assessed during the study. (A) coffee leaf rust (caused

by Hemileia vastatrix) spores on the underside of the leaf, (B) mummified coffee beans as a

28
result of coffee berry disease (caused by Colletotrichum kahawae), (C) blue-black

discoloration of the stem as a result of coffee wilt disease (caused by Gibberella xylarioides),

and (D) stem cracking and rhizomorph growth in the cracked stem due to infection by

Armillaria root rot (caused by Armillaria mellea).

29
30
Fig. 3. The relationship between altitude, shade canopy cover and coffee structure index and

the severity of: (A-C) coffee leaf rust (Hemileia vastatrix), (D-F) coffee berry disease

(Colletotrichum kahawae), (G-I) coffee wilt disease (Gibberella xylarioides) and (J-L)

Armillaria root rot. For coffee leaf rust and coffee berry disease, data points shown are the

proportion of leaves/berries with coffee leaf rust/coffee berry disease infection, as averaged

across the 16 coffee shrubs per site. For coffee wilt disease and Armillaria root rot, data

points shown are proportions of coffee shrubs with their respective disease symptoms per site

(50 × 50 m). Linear trend lines are superimposed on the graphs when the relationship for the

variable was significant at p < 0.05 in the GLM(M)s. See Table 3 for the statistical summaries

from the final models.

31
Table 1. Environmental and stand structure variables quantified in each of the sixty study

sites. The coffee structure index reflects coffee tree architecture (growth habit) as a result of

different management (see the Methods section for details) and the management index

captures the common management activities within the different coffee systems (See

appendix). Environmental variables are measured within 30 × 30 m plots (except shade trees,

which were measured in a 50 × 50 m area), and values in brackets are estimates per hectare.

Variables Min. Max. Mean SD

Canopy cover (%) 13 83 52 16
Canopy layers (number) 1 2 3 0.8
Coffee shrub density (>1.5 m) (number/ha) 107 (1189) 1101 (12233) 351 (3900) 178
Coffee structure index (see Methods section) 1 3 2 0.5
Management index (See appendix) 0.33 1.67 0.77 0.40
Shade trees >20 cm DBH (number/ha) 5 (20) 43 (172) 22 (88) 9
Surrounding forest area within 1 km buffer (km2) 0.16 3.22 1.58 0.73
Proportion of non-coffee shrubs to coffee (%) 0 32 5 8
Altitude (m a.s.l.) 1506 2159 1851 174
Slope (%) 1 24 11 5

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Table 2. Site-level variation in disease levels and the relative amount of variation in disease

levels present among sites and among shrubs within sites (see methods section). Values for

coffee leaf rust are based on the mean proportion of leaves with leaf rust averaged across all

16 shrubs per site. Values for coffee berry disease are based on; i) branches with coffee berry

disease – mean proportion of number of bearing branches with coffee berry disease and ii)

berries with coffee berry disease – mean proportion of berries with coffee berry disease from

16 shrubs per site. Values for coffee wilt disease and Armillaria root rot are based on the

proportion of coffee shrubs with their respective disease symptoms per site. For all the four

diseases, the proportions are converted to percentages.

Min. Max Mean Variation Variation

Diseases
(%) (%) (%) among sites (%) within-site (%)
Coffee leaf rust 0.1 35.1 9.28 12 88
Coffee berry disease
i) berries with coffee berry disease 0 45.7 7.50 57 43
ii) branches with coffee berry disease 0 20.7 3.85 48 52
Coffee wilt disease 0 5.26 1.47 - -
Armillaria root rot 0 5.38 0.53 - -

33
Table 3. Summary of the relationship between abiotic and biotic environment and management intensity and incidence and severity of the four

major fungal diseases of coffee. Shown are χ2-values and standard regression coefficients (SC) from the minimum adequate model (except *), as

estimated from generalized linear (mixed) models.

Shade Shade trees Proportion of Coffee Surrounding tree

canopy >20 cm Coffee non-coffee to structure cover (km2) Surveying
Response variables Altitude Slope cover (DBH) density coffee shrubs index date
Coffee leaf rust χ2 = 47.38 - χ2 = 5.74* - - - - χ2 = 5.18 χ2 = 26.53
severity p < 0.001 - p = 0.017* - - - - p = 0.023 p < 0.001
SC = -0.64 - SC = -0.30* - - - - SC = 0.20 SC = -0.45

Berries with coffee χ2 = 23.76 - - - - - χ2 = 7.03 - -

berry disease p < 0.001 - - - - - p = 0.008 - -
SC = 1.62 - - - - - SC = -0.77 - -

χ2 = 22.46 - - - - - χ2 = 8.81 - -
Branches with p < 0.001 - - - - - p = 0.003 - -
coffee berry disease SC = 1.34 - - - - - SC = -0.73 - -

χ2 = 45.09* - χ2 = 8.90 χ2 = 66.80 χ2 = 59.93 - - - -

Coffee wilt disease p < 0.001* - p = 0.003 p < 0.001 p < 0.001 - - - -
SC = 0.28* - SC = 0.12 SC = 0.34 SC = -0.24 - - - -

χ2 = 27.60 - χ2 = 15.23 χ2 = 94.75 χ2 = 17.34 - χ2 = 212.04 - -

Armillaria root rot p < 0.001 - p < 0.001 p < 0.001 p < 0.001 - p < 0.001 - -
SC = 0.43 - SC = -0.34 SC = 0.81 SC = -0.33 - SC = 1.00 - -
* Values from individual regression models

34