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RESEARCH PAPER
Tree diversity and shade rate in complex cocoa-based
agroforests affect citrus foot rot disease
Akoutou Mvondo Etiennea,b,*, Ndo Eunice Golda Danielea,
Bidzanga Nomo Luciena, Ambang Zacheeb, Bella Manga Faustina, Cilas Christianc
aInstitute of Agricultural Research for development (IRAD), P.O. Box 2123, Yaounde, Cameroon
bDepartment of Plant Biology and Physiology, Faculty of Science, University of Yaounde I, P.O. Box 812, Yaounde,
Cameroon
cCIRAD, UPR Bioagresseurs, 34398 Montpellier, France
Received 2 September 2021; accepted 7 August 2022
Available online 9 August 2022
Abstract
The role of agroforest systems in pathogen regulation through structural characteristics such as shade and tree diversity is rec-
ognized. However, few studies have examined the importance of these factors on the spread of diseases of associated fruit trees
in agroforestry systems, especially cocoa-based agroforestry systems (CBAS). The aim of this study was to evaluate the effect
of associated tree diversity and shade rate into CBAS on citrus Phytophthora foot rot disease (PFRD) intensity. The study was
carried out in five citrus production basins of Cameroon, contrasted by ecology and rainfall regimes. A set of 33 CBAS plots
was mapped and their species composition and vertical structure were determined. Field data were used to reconstruct CBAS
in 3D with Shademotion 5.1.47 software. Using static simulations with shadow overlays, shade rate received by each citrus
tree was calculated. Subsequently, citrus trees were grouped into three categories according to the shade rate they received: (i)
full sun, with shade rate <30%; (ii) light shade with shade rate 3070% and, (iii) dense shade, with shade rate >70%. PFRD
intensity was determined by measuring the canker extent relatively to the citrus crown circumference. A significant difference
in PFRD intensity was observed between the different shade rates. Citrus trees receiving no shade were significantly more
attacked by PFRD than those receiving little shade or dense shade. The antagonistic effect of shade was demonstrated. At the
expense of factors related to the specific composition of the CBAS, shade, temperature, relative humidity and rainfall were
found to be the main factors explaining PFRD intensity in CBAS. This study shows that microclimatic alterations due to the
biodiversity in tropical agroforestry systems contribute to sustainable pest management.
© 2022 The Authors. Published by Elsevier GmbH on behalf of Gesellschaft für Ökologie. This is an open access article under
the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
Keywords: Agroforestry; Biodiversity; Phytophthora; Citrus, and integrated disease management
Introduction
Conventional agriculture has allowed for the tremendous
increase in agricultural production since the 1950s, contrib-
uting to the relative reduction of hunger and poverty glob-
ally (Pingali, 2012). However, the resulting heavy
*Corresponding author at: Institute of Agricultural Research for develop-
ment (IRAD), P.O. Box 2123, Yaounde, Cameroon.
E-mail address: etienneakoutou@gmail.com (A.M. Etienne).
https://doi.org/10.1016/j.baae.2022.08.003
1439-1791/© 2022 The Authors. Published by Elsevier GmbH on behalf of Gesellschaft für Ökologie. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
Basic and Applied Ecology 64 (2022) 134146 www.elsevier.com/locate/baae
ecological toll discredits this model of agriculture and makes
it unsustainable (Jepson et al., 2014; Sharma et al., 2019).
The chemical plant protection products extensively used in
conventional agriculture have drastic effects on non-target
species and affect animal and plant biodiversity, as well as
aquatic and terrestrial food webs (Tudi et al., 2021). The use
of chemical plant protection products is thus of increasing
concern for both agriculture itself and the environment as
well as human and animal health (Warra & Prasad, 2020).
Improving agricultural production systems toward new
models of sustainable, resilient, and environmentally-
friendly agriculture is becoming an urgent need (Dornbush
& von Haden, 2017).
The agroecological strategy of relying on ecological pro-
cesses of interest, within agroecosystems, to maximize pro-
ductivity and sustainability, while reducing the use of
chemical inputs is gaining acceptance. Agroecosystems thus
represent a preferred pathway to resilient and future agricul-
tural systems (Bennett et al., 2021). Indeed, inspired by nat-
ural ecosystems, which are the result of an adaptation of
animal and plant communities in a given environment, and
thus to specific biotic and abiotic constraints, these systems
provide a model for sustainability and resilience (Ngo Bieng
et al., 2013). Among these characteristics of natural ecosys-
tems, species diversity is assumed to play a key role in the
sustainability and multifunctionality of agroforestry sys-
tems. Thus, an increase in plant diversity in agroecosystems
is assumed to improve the provision of many ecosystem
services, including pest regulation (Schreefel et al., 2020)
Agroforestry is a dynamic and ecological resource man-
agement system that, through the integration of trees into
agricultural and rangelands, diversifies and sustains small-
holder production for increased socio-economic and envi-
ronmental benefits. In recent decades, various studies have
described and characterized the structure of cocoa-based
agroforestry systems (CBAS) (Akoutou Mvondo et al.,
2020; Gidoin et al., 2014). In the Cameroonian rainforest
areas, citrus trees are mainly produced in CBAS (Akoutou
Mvondo et al., 2019; Ndo, 2011). Although various citrus
species/varieties are grown in Cameroon, the main species
found are C. sinensis, C. reticulata, C. paradisi, C. maxima
and C. limon (Fig.1A).
In agroforestry, the term shading is related to the microcli-
matic alterations that occur in the understory due to the pres-
ence of an upper vegetation canopy in the agroforestry
system. The presence of trees associated with a crop buffers
air and soil temperature, decreases wind speed and the quan-
tity and quality of transmitted light ; and increases relative
air humidity and soil moisture in the understory (Tscharntke
et al., 2011). The effect of shading on pests is controversial
(Schroth et al., 2000). While dense shade favours the spread
of some pathogens, light shade or no shade may limit the
development of other pathogens (Akoutou Mvondo et al.,
2019). Several studies have shown the implication of shad-
ing on the development and spread of various pathogens
(Durand-Bessart et al., 2020). The effects of shade have
been documented; and light, especially ultraviolet light has
been shown to stimulate sporulation of many fungal species.
In addition, microclimate can indirectly influence pathogen
through its impact on the host plants (Pumari~no et al.,
2015).
Phytophthora are important soil and waterborne patho-
gens responsible for significant damage in agricultural and
natural ecosystems. The genus Phytophthora represents a
significant and emerging biosecurity threat worldwide
(Puglisi et al., 2017). To nowadays, about 182 Phytophthora
species have been formally described, with an estimated
total of 326 species covering 12 phylogenetic clades (Bose
et al., 2021). Of these Phytophthora species, about 13 infest
citrus (Asim et al., 2019). P. nicotiana (Syn. P. parasitica),
P. palmivora and P. citrophthora are the most damaging
species worldwide and are therefore the most economically
important (Gade & Lad, 2019). Phytophthora foot rot dis-
ease (PFRD) is thus a major constraint and a global concern
for the citrus industry (Ramallo et al., 2019;Chaudhary et
al., 2020). Phytophthora losses on citrus result from seed-
ling dieback in the germplasm, root and crown rots in the
nursery and in field. Foliage dieback resulting from root rot
precipitates tree death and limits orchard life span. Pre- and
post-harvest fruit rots also result in huge production losses
(Graham & Feichtenberger, 2015). Among these symptoms,
citrus Phytophthora foot rot disease (PFRD) is the most
severe, and causing the most damage in the major citrus pro-
ducing areas, as well as in Cameroon (Fig. 1B and C)
(Akoutou Mvondo et al., 2019, 2020).
PFRD managing requires a complex and costly set of
strategies (Gade & Lad, 2019). Of all these methods, the
chemical control approach is the most widely used in the
major citrus growing areas (Sawake et al., 2022). In Came-
roon, however, most citrus production is provided by small-
holders, for whom these methods are not feasible and too
expensive. Production systems have remained traditional,
and cultural practices empirical (Ndo, 2011). Citrus varieties
used are not always tolerant to PFRD, and plots were estab-
lished with ungrafted seedlings. In addition, ever-increasing
concerns about environmental and soil health are driving the
search for more environmentally friendly means of disease
control (Panth et al., 2020). Thus, there is an urgent need to
develop targeted PFRD management strategies tailored to
local production systems and context. This paper aims to
evaluate the effect of floristic diversity in CBAS and the
resulting shade rate on PFRD intensity. The basic hypothesis
is that microclimatic alterations in CBAS contribute to
reducing the intensity of PFRD.
Materials and methods
Study area and citrus production basins
Five citrus production basins (CPB) were selected from
four different ecologies:
A.M. Etienne et al. / Basic and Applied Ecology 64 (2022) 134146 135
 Bokito CPB (Latitude: 4° 330 59.9900 N; Longitude: 11° 060 60.0000 E),
located in the forest-savanna transition zone. The climate is hot and
humid, with average annual temperature of 25.5 °C, average rainfall of
831.7 mm with a bimodal pattern, and an average relative humidity of
75%. CBAS are usually established in previous cropping areas (Jagoret
et al., 2012b, 2018). Given the scarcity of native forest trees, fruit trees
are abundantly introduced to provide shade for cocoa trees and are
considered as valuable source of income.
 Evodoula CPB (latitude: 011°140592 ''E; longitude: 04°060226 ''N),
located in the degraded forest zone. The climate is hot and humid, tem-
peratures around 23.0 °C, average rainfall of 1727 mm with a bimodal
pattern, and an average relative humidity of 85%. This site is located
in the Lekie Sub-division which is currently the largest cocoa-produc-
ing area in Cameroon. Cocoa is produced in complex and highly biodi-
verse CBAS. Fruit trees, including citrus, are an essential component
of these CBAS;
 Bikok (Latitude: 3° 380 31.31 ''N; Longitude: 11° 310 54.88 ''E) and
Boumnyebel (Latitude: 3° 520 59.500 N; Longitude: 10° 510 00.800 E)
CPBs are located in the dense forest zone. The climate is hot and
humid, temperatures around 25.7 °C, average rainfall of 1800 mm
with a bimodal pattern, and an average relative humidity of 84%.
These two CPBs are different from each other, particularly in terms of
the crops grown by the local populations. In Bikok, cocoa farming is
practiced in complex and highly biodiverse CBAS, whereas in the
Boumnyebel, farmers practice oil palm production in addition to cocoa
farming. Thus, in the latter CPB, it is very common to find palm trees
associated not only with cocoa trees, but also with fruit trees such as
citrus;
 Muyuka CPB (Latitude: 4° 170 23.2800 N; Longitude: 9° 240 37.0800 E),
located in the humid forest zone with monomodal rainfall. It is a very
humid and hot dense forest area, with average annual temperatures
ranging from 22 to 29 °C and relative humidity of 85 to 95%. The
average annual rainfall varies from 2500 to 4000 mm and even
11,000 mm in some localities. It is characterized by a 3-month dry sea-
son (December to February) and a 9-month rainy season (March to
November). Muyuka represents one of the largest cocoa production
basins in Cameroon (Mukete et al., 2018). Here, cocoa production is
intensive and farms are managed in such a way as to optimize cocoa
production. this is done in particular by reducing the number of associ-
ated trees. It has been shown that in this locality CBAS tend to be bi-
specific, associating cocoa and fruit trees, generally citrus (Akoutou
Mvondo et al., 2019).
Across all of the CPBs, 33 plots were established includ-
ing eight in Bokito, seven each in Bikok and Evodoula, six
in Muyuka, and five in Boumnyebel. Each CPB represents a
geographical area with fairly homogeneous climatic and
edaphic conditions and can therefore guarantee homoge-
neous citrus production. Within each CPB, study plots were
at least 3 km apart. In each CPB, CBAS plots with (i) at least
12 citrus trees (including all citrus species) on a surface of
2500 m2, (ii) diverse forest trees and (iii) fruit trees other
than citrus, were selected.
Mapping of CBAS and tree characterization
CBAS mapping essentially consisted of taking the x and y
coordinates of perennial plants present in the sample area in
order to reconstruct CBAS and quantify shade rate. Mapping
Fig. 1. Illustration of (A) an orange tree (Citrus sinensis) planted in a complex cocoa-based agroforest; (B) an orange tree attacked by Phy-
tophthora foot rot disease; (C) and a mandarin tree (C. reticulata) completely declined following a severe attack of the Phytophthora foot rot
disease.
136 A.M. Etienne et al. / Basic and Applied Ecology 64 (2022) 134146