Science of the Total Environment 899 (2023) 165657 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Combined effects of shade and drought on physiology, growth, and yield of mature cocoa trees Eric Opoku Mensah a,b,g,*, Anders Ræbild b, Richard Asare c, Christiana A. Amoatey a, Bo Markussen e, Kwadwo Owusu f, Bismark Kwesi Asitoakor a,b,g, Philippe Vaast d,h a Department of Crop Science, University of Ghana, Legon, Accra, Ghana b Department of Geosciences and Natural Resource Management, University of Copenhagen, Denmark c International Institute of Tropical Agriculture (IITA), PMB, L56, Legon, Accra, Ghana d UMR Eco & Sols. Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), Université Montpellier, Montpellier, France e Department of Mathematical Sciences, University of Copenhagen, Denmark f Department of Geography and Resources Development, University of Ghana, Legon, Accra, Ghana g CSIR-Plant Genetic Resources Research Institute, P. O. Box 7, Bunso, Eastern Region, Ghana h World Agroforestry Centre (ICRAF), Nairobi, Kenya H I G H L I G H T S G R A P H I C A L A B S T R A C T • Effects of shade and rainwater suppres- sion were studied on mature cocoa trees. • Rainwater suppression led to drought and decreased performances of the cocoa trees. • Shade enhanced physiology, growth, and yield of the cocoa trees than the full sun. • Shade will benefit cocoa but will not save it from negative effects of drought. A R T I C L E I N F O A B S T R A C T Editor: Elena Paoletti Climate models predict decreasing precipitation and increasing air temperature, causing concern for the future of cocoa in the major producing regions worldwide. It has been suggested that shade could alleviate stress by Keywords: reducing radiation intensity and conserving soil moisture, but few on-farm cocoa studies are testing this hy- Agroforestry pothesis. Here, for 33 months, we subjected twelve-year cocoa plants in Ghana to three levels of rainwater Carbon accumulation suppression (full rainwater, 1/3 rainwater suppression and 2/3 rainwater suppression) under full sun or 40 % Climate change Cocoa uniform shade in a split plot design, monitoring soil moisture, physiological parameters, growth, and yield. 3 − 3 Drought adaptation Volumetric soil moisture (ϴw) contents in the treatments ranged between 0.20 and 0.45 m m and increased Shade under shade. Rainwater suppression decreased leaf water potentials (ѱw), reaching − 1.5 MPa in full sun con- ditions indicating severe drought. Stomatal conductance (gs) was decreased under the full sun but was not affected by rainwater suppression, illustrating the limited control of water loss in cocoa plants. Although pre- dawn chlorophyll fluorescence (Fv/Fm) indicated photoinhibition, rates of photosynthesis (Pn) were highest in * Corresponding author at: CSIR-Plant Genetic Resources Research Institute, P. O. Box 7, Bunso, Eastern Region, Ghana. E-mail address: eom@ign.ku.dk (E.O. Mensah). https://doi.org/10.1016/j.scitotenv.2023.165657 Received 7 May 2023; Received in revised form 26 June 2023; Accepted 17 July 2023 Available online 20 July 2023 0048-9697/© 2023 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). E.O. Mensah et al. S c i e n c e o f t h e T o t a l E n v i r o n m e n t 899 (2023) 165657 full sun. On the other hand, litter fall was highest in the full sun and under water stress, while diameter growth and carbon accumulation increased in the shade but was negatively affected by rainwater suppression. Abortion of fruits and damage to pods were high under shade, but dry bean yield was higher compared to under the full sun. The absence of interactions between shade treatments and rainwater suppression suggests that shade may improve the performance of cocoa, but not sufficiently to counteract the negative effects of water stress under field conditions. 1. Introduction increased production of assimilates and growth (Galyuon et al., 1996; Acheampong et al., 2013; Mensah et al., 2022). However, other studies Cocoa (Theobroma cacao L.) is a shade-adapted plant that grows well point to negative effects of agroforestry under extreme drought (Moser in humid tropical conditions with regular rains and a short dry season et al., 2010; Abdulai et al., 2017; Gateau-Rey et al., 2018). Reductions in (Pohlan and Perez, 2010), requiring a minimum of 1200 mm of water yield and mortality of cocoa trees may be due to belowground compe- per year (Zuidema et al., 2005; Ameyaw et al., 2018). An extended dry tition for both water and nutrients, aside from effects of reduced radi- period exceeding three months can reduce tree growth and yield of ation. Competition for soil water and nutrients can be reduced by cocoa (Lahive et al., 2019) and cocoa thrives best when rain distribution selecting the right species and/or management of shade (Asitoakor et al., is uniform along the year (Carr and Lockwood, 2011). About 70 % of the 2022; Rigal et al., 2022), but it is unclear whether shade may play a cocoa is produced in regions where most of the farms are rain-fed and positive role for cocoa trees subjected to drought stress. Recently, we characterized by 4–5 dry months (rainfall<100 mm) (Wessel et al., showed that shade improved the physiological performance of cocoa 2015; Ruf et al., 2015; Lahive et al., 2019) indicating vulnerability of the seedlings but had limited effects on the response to high temperature cocoa tree to an already existing drought condition. This could explain stress (Mensah et al., 2022). Here, we investigate the hypothesis that why most of the cocoa farms are performing below the potential output, shade reduces negative effects of drought on physiology, growth, and such as in West Africa where average yields are between 400 and 700 kg yield of cocoa trees. To test our hypothesis, we performed an ecosystem ha− 1 while potential yields in the sub-region are reported to be around manipulation trial where mature cocoa trees were drought stressed by 2000 kg ha− 1 and up to 6000 kg ha− 1 in other regions (Aneani and Ofori- rainfall interception, while exposing them to full sun or uniform shade Frimpong, 2013; Van Vliet and Giller, 2017; Bymolt et al., 2018; Asante using artificial shade nets. et al., 2022). Climate projections foresee increases in frequency and severity of droughts (Läderach et al., 2013; Sylla et al., 2016; Ahma- 2. Experimental design dalipour et al., 2019), which causes concern for vulnerable cocoa famers who have limited adaptive capacity to cope with the impact of weather The experiment was conducted from April 2018 to March 2021 in a events (Brian et al., 2022). Drought was causing an estimated 27 % yield homogeneous, unshaded field at a cocoa farm in the Western North Region loss in West Africa in the 1980s (Schroth et al., 2016) and is suggested to of Ghana (2o33’W, 6o23’N, 165 m a.s.l). The site falls within the moist be the most serious threat to cocoa production (Carr and Lockwood, semi-deciduous forest zone. At the start of the experiment, the cocoa plants 2011). Responses to drought range from lower leaf transpiration rates were 12 years old, 4.5 m tall and had an average diameter at breast height and stomatal conductance of plants over decreased bean yields to death (DBH) of 8.5 cm. Spacing between the trees was on average 3 × 3 m. of trees (Rada et al., 2005; Schwendenmann et al., 2010; Abdulai et al., A two-factor split plot design was used. The main plots consisted of 2017; Gateau-Rey et al., 2018), confirming the negative effects of two levels of shade (40 % shade and full sun) while the subplots con- drought on cocoa production across the globe. sisted of three levels of rainwater suppression (full rainwater as control, Drought occurs when soil water is reduced to the extent that plants 1/3 rainwater suppression, and 2/3 rainwater suppression). Selection of can no longer extract sufficient water for normal life processes (Coder, 40 % shade was based on earlier recommendations by Asare and David 2018). High transpiration through the leaves but limited root water (2010) and Andres et al. (2018). The 1/3 and the 2/3 rainwater sup- supply to the plants creates an imbalance (Anjum et al., 2011; Lamaoui pression levels were chosen to ensure that cocoa plants would be water et al., 2018) causing a reduced flow of water through the xylem to stressed. As we did not control stemflow and possible lateral movements nearby cells and highly negative pressures in the xylem. Cell turgor of water in the soil, we covered a larger proportion of the soil, expecting declines, impairing the division and elongation of cells (Fahad et al., that this would result in a less-than-proportional reduction in soil water. 2017), resulting in reduced growth and yield. Plants respond by sto- The design was replicated in three blocks. Provision of shade was ach- matal closure, limiting water loss, CO2 uptake and thus photosynthesis ieved using a shade net with a shading capacity of 40 % (Fig. 1A) raised (Feller and Vaseva, 2014; Baligar et al., 2017). This reduces the pro- above the cocoa canopy at 6.5 m from the ground. duction of assimilates and affects partitioning to reproductive organs. Flat and slightly pending panels were raised in the rows of the cocoa Thus, long drought periods impact flower production (Handley, 2016; trees at a height of 1 m, covered with plastic sheets (350 μm plane plastic Wuriandani et al., 2018) and cause flower abortion, reducing survival of sheets, Poly-products, Ghana) to lead the rainwater away from the plots pollinated flowers (Frimpong-Anin et al., 2014), pods sizes (Handley, (Fig. 1B). 2016) and dry bean yield in cocoa (Abdulai et al., 2018; Gateau-Rey In the 2/3 rainwater suppression treatment, the panels covered et al., 2018). The number of beans per pod, bean size, and weight are approximately 2/3 of the ground, while in the 1/3 rainwater treatments, also reduced by drought (Handley, 2016). about 1/3 of the ground surface was covered. Trenches were dug and Cocoa agroforestry is receiving increasing interest because yields are lined with aluminium sheets leading the collected rainwater at least 10 often higher under shade when fertilizer inputs are low (Ahenkora et al., m away from the treated plots. Each of the three blocks thus had six 1974; Baligar et al., 2008; Asare et al., 2016). In addition, shade trees subplots (each subplot measuring 15 × 15 m and with 25 cocoa plants) enhance functional biodiversity including sequestration of carbon, including the six combinations of shade and rainwater suppression management of soil fertility and weeds, and biological control of pests levels, resulting in a total of 18 subplots covering 0.5 ha. Main plots were and diseases (Wessel, 2001; Vaast and Somarriba, 2014; Vaast et al., surrounded by two border rows to eliminate border effects. Shade nets 2016). As in other species, shade protects the photosynthetic machinery were installed the first time in July 2018 and water exclusion panels in from photoinhibition (a condition that occurs under excessive light and October 2018. However, due to strong winds and mounting problems, degrades photosystem II), resulting in high photochemical efficiency blowing down shade nets and panels, they were fully effective from May and rate of electron transport of cocoa under shade, thus contributing to 2019 and for the rest of the experiment (Fig. A.1). 2 E.O. Mensah et al. S c i e n c e o f t h e T o t a l E n v i r o n m e n t 899 (2023) 165657 Fig. 1. A) Shade nets providing 40 % shade suspended above the cocoa plants and B) Plastic sheets covering the spaces between cocoa plants to reduce precipitation. Photos: Eric Opoku Mensah, 2020. All measurements were collected on the fourth matured leaf from the from 0 to 10 cm and clayey through the rest of the profile down to 160 top phyllotaxy selected from three top or peripheral branches from the 9 cm (Determined at Soil Science Department, University of Ghana ac- middle plants in each subplot (n = 9 plants for 6 treatments and 3 repli- cording to Beretta et al., 2014) while bulk density varied between 1.4 cates, totalling N = 162), using ladders to access the top of the crown. and 1.7 g cm− 3 along the soil profile. Soil organic carbon, % total ni- trogen and phosphorus were low (Table A.1). Application of Asaase wura cocoa fertilizer (an NPK fertilizer with 0–22-18 + 9CaO + 7S + 6MgO 2.1. Agronomic practices formulation) was done through broadcasting in May 2018 at a recom- mended rate of 400 kg ha− 1. Ammonium sulphate was placed in shallow The cocoa plants were pruned in April 2018 during the start of the basins around the trees at 70 g tree− 1 and about 40 cm from the base of experiment under a government-initiative program. Vertical shoots the trees in May 2019 corresponding to 78 kg ha− 1. The NPK application (chupons) were subsequently removed when observed. Weed control was repeated in June 2020. was achieved by slashing every two months during the rainy season (April – October) and every three months during the dry season (November – March). Control of mirids (Sahlbergella singularis, Distant- 2.2. Environmental parameters iella theobroma, Helopeltis spp.) and other insects were done three times during the year; February, July, and September using Confidor (Imida- A weather station including a photosynthetic active radiation (PAR) clopid; Kumark Company Limited, Ghana) and Akatsi master (Bifen- sensor (S-LIA-M003), temperature/RH smart sensor (S-THB-MOO8), thrin; Chemico Ltd., Ghana) at the recommended rates of 150 ml ha− 1 rain gauge sensor (S-RGx-M002) and HOBO data logger (H21-USB) and 500 ml ha− 1, respectively (Baah et al., 2016). Black pod diseases (Onset Computer Corporation, USA) was installed in the nearby village, (Phytophthora megakarya, P. palmivora) were controlled in July and in two kilometres away from the experimental site, and readings registered September every year using Ridomil Gold 66 WP (copper oxychloride every 10 min. One hygrochron ibutton ((DS1923-F5 hygrochron, ibut- and mefenoxam; Syngenta, Australia) at a rate of 50 g per 15 l of water. ton Link, United States) per block was hung below the cocoa canopy in Regular removal of damaged and spotted pods was undertaken to reduce the control plots 1.5 m above the soil surface, monitoring below canopy fungal sporulation. Parasitic mistletoes (Tapinanthus bangwensis) were temperature and relative humidity every 10 min. Vapour pressure removed with cutlasses regularly. deficit (VPD) was calculated from temperature and relative humidity A composite soil sample was collected at the onset of the experiment readings according to Howell and Donald (1995). The ibuttons were and analysed. Soil textural analysis showed that the soil was a sandy clay shielded under plastic bowls covered with aluminium foil. 3 E.O. Mensah et al. S c i e n c e o f t h e T o t a l E n v i r o n m e n t 899 (2023) 165657 Soil water content was monitored every second week from Effects of shade and rainwater suppression on carbon accumulation September 2019 to March 2021 with a Diviner soil moisture probe were determined from the aboveground biomass (AGB) of the cocoa (Diviner 2000 Series II, Sentek Soil Moisture Sensors, Sentek Technol- plants. AGB was calculated using the allometric equation for tropical ogies, South Australia) using PVC pipes (NJPLAST GH uPVC 2″). Fifty- trees proposed by Chave et al. (2014) where AGBtree = 0.0673 x four pipes were installed in the field with equal distributions among (ρD2 0.976150H) , ρ = tree density (0.42 g cm− 3 for cocoa as indicated by the treatments. Volumetric moisture content was determined using the Chave et al., 2006 and Wade et al., 2010); D150 = initial diameter (at manufacturer's generic equations every 10 cm down to the 130 cm soil 150 cm-height) of the cocoa trees collected before the start of the depth except sites with rocky pans, where measurements were moni- treatments plus the stem expansion (cm) taken from the dendrometer tored only to 90 cm soil depth. band readings at the last month of rainwater suppression; The H in the equation is the average cocoa tree height (m) at the start of the exper- 2.3. Physiology iment. We assumed that the stem expansion where the dendrometer bands were placed was equivalent to the stem expansion at the D150, and Leaf water potential was measured using a field Scholander pressure that tree height did not increase during the experiment. The latter may chamber (Pump-Up Chamber Instrument, PMS Instruments, USA) start- have led to an underestimation of C accumulations in the cocoa plants ing from November 2018 to December 2020. All measurements were after the treatments. AGB of the cocoa trees was converted into Mg ha− 1 taken at predawn (4,00–5:30 am) (Avila-Lovera et al., 2016), using small by using the average spacing between trees (Macias et al., 2017; Afele stems of about 1 mm thickness from the upper or peripheral branches et al., 2021). Carbon accumulation was calculated as AGB * Fc; where Fc from three selected plants in the middle row per subplot every month. = 0.5 (Fc = carbon fraction) (IPCC, 2003; Somarriba et al., 2013). Diurnal trends of water potential were assessed in January, April, July, September, and December of 2019 and 2020 at five different time points (around 5:00 am, 9:00 am, 12:00 am, 3:00 pm and 6:00 pm). 2.5. Yield Measurements were done after leaves were sealed in aluminium foil for 30 min, over three-day periods with one block per day. Flower production and canopy density were assessed on a visual Non-destructive measurements of rate of net photosynthesis (P ), scale from 0 to 5; a score of zero indicated no flowers or no leaves and a n transpiration (E), stomatal conductance (gs), sub-stomatal CO concen- score of 5 indicated maximum flowering intensity or a dense canopy. 2 tration (Ci) and photosynthetic active radiation (PAR) were conducted These assessments were conducted on the middle nine trees of each with a CIRAS-3 portable gas analyser (PP systems, USA) in September subplot. The total number of individual flowers produced per tree was 2019, December 2019, February 2020, April 2020, July 2020, and quantified by estimating the number of flower cushions and the number September 2020 between 10 am – 11 am. The fourth fully developed leaf of flowers per cushion at the section of the stem from 50 to 150 cm from of three selected branches from the top or the periphery of four selected the base of the tree. The estimates were based on images (Fig. A.2) of middle plants per subplot were used for the measurements. Water use stems of ten plants, selected because of their differences in flowering efficiency (mmol mol− 1) was calculated as the ratio of photosynthesis to intensity score during the peak flowering month (July 2018). On these transpiration. Measurements lasted for three days with one block per trees, the number of flower cushions was counted and averaged for each day, using natural light conditions with CO2 set at 400 ± 10 μmol mol− 1, level of score. The number of individual flowers of a flower cushion of cuvette temperature at 28 ± 1 ◦C, 50 % of the ambient humidity and one hundred randomly selected cushions was counted and averaged cuvette flow at 300 cm− 3 min− 1. (Average number of individual flowers per cushion = 16). The total The ratio of variable to maximal chlorophyll florescence (F /F number of flowers per plant along the selected part of the stem was then v m) was measured using a mini-PAM photosynthesis yield analyser (Portable calculated as the product of the number of flower cushions per score per Chlorophyll Fluorometer - Heinz Walz GmbH, Germany) in darkness plant and the average number of individual flowers per cushion. Flower from 4:30–5:30 am in the same months as gas exchange was measured. production was measured monthly on the middle nine plants of each Minimum fluorescence in dark-adapted state (F ) was read with a subplot from September 2018 to March 2021. o measuring beam at low light intensity (<0.02μmolm− 2 s− 1) while Young pods (≤6 cm length or ≤ 3 cm width) were considered as maximum fluorescence in dark-adapted state (F ) was obtained after a cherelles. The numbers of healthy and dead cherelles on the stem from m saturating pulse was applied (about 5500 μmolm− 2 s− 1 PAR for a 50 to 150 cm from the base were counted monthly to assess the transi- duration of 0.7 s) (Chen et al., 2012). Variable fluorescence (F ) was tion of flowers to cherelles and pod formation. Damaged pods and v calculated as the difference between F and F (F = F - F ) while aborted cherelles were removed after each monthly count of the cher-m o v m o maximum photochemical efficiency of the photosystem II was deter- elles. Finally, the total number of pods on the whole tree was counted, mined as F /F = (F – F )/F . followed by harvesting and recounting of healthy ripe pods to determine v m m o m pod yield per tree. 2.4. Litter fall, stem growth and carbon accumulation Weight, length, and width of pods were measured on ten randomly selected pods per subplot after each harvest during the peak harvesting Plant litter fall was collected from October 2018 to December 2020. months (September, October, and November from September 2018 to Four wooden boxes of 0.25 m2 base area and 0.5 m height (Ofori-Frim- March 2021). The number of beans per pod excluding the pulps was pong et al., 2007; Brando et al., 2008; Triadiati et al., 2011) were placed counted and weighed. After weighing, beans were pooled per subplot on each subplot between the middle nine plants (Dawoe et al., 2010; and the weight of 100 randomly selected beans was recorded. Beans Paudel et al., 2015). Each litter box was placed on bamboo sticks 5 cm were treated separately for each subplot and were covered with plantain above the soil surface to prevent decay. Litter from the four boxes per leaves, labelled, and kept under a heap of cocoa beans for fermentation subplot were pooled monthly, oven dried at 70 ◦C for 48 h (Schwen- for six days. Beans were then sun-dried for seven days and weighed to denmann et al., 2010) and weighed to measure biomass leaf yield per compute dry bean yield per hectare and season (two seasons annually, treatment. with the major season being from September the previous year to March Dendrometer bands (DBM80 manual band dendrometer, ICT Inter- the following year, while the minor season was from April to August in national) were placed around the stems of two plants from each subplot the same year), following a modified model of Lachenaud (1984) and to measure stem expansion at 90 cm from the base of the stem. Growth of Wibaux et al. (2017): stem was observed using the sliding spring scale on the bands, m x NPH x NBP x MDB(g) measuring between 10 and 11 am monthly from November 2018 to Y = n x 1000g x kg− 1. December 2020. 4 E.O. Mensah et al. S c i e n c e o f t h e T o t a l E n v i r o n m e n t 899 (2023) 165657 where; compared to full sun plots while VPD were 0.04–0.28 kPa higher in the Y = Yield− 1ha− 1season− 1 (kg ha− 1 season− 1) full sun (Fig. A.5). Neither relative humidity nor temperatures were m Total number of trees per hectare (1110 trees per hectare with 3 affected by the rainwater suppression treatments (Table A.2). = m 3 m planting distance) Plant water potential (ѱw) at predawn was significantly affected by × n Number of trees used for yield measurements (n 9) shade, rainwater suppression and day of measurements. Under shade, = = NPH = Average number of healthy pods harvested per season ѱw values ranged between - 0.7 and - 0.15 and were between 0.14 and NBP Average number of beans per pod 0.05 MPa higher than the values obtained in the full sun plots during the = MDB Average mass per dry bean wet months and between 0.28 and 0.06 MPa higher during the dry = 1000 g kg− 1 Factor to convert yield in g to yield in kg months (Table A.2, Fig. 2). Among the rainwater suppression treat-= ments, leaf water potential was very low in the 2/3 rainwater suppres- sion plots compared with the 0/3 and the 1/3 plots. For example, 2/3 2.6. Data analyses rainwater suppression plots in the full sun showed ѱw values as low as − 0.9 MPa compared with the full rainwater plots with − 0.6 MPa in the The statistical analyses fall into 3 groups depending on the sampling same month. schemes. The first group investigated the influence of shade (2 levels: Water potentials were more negative in the dry months between full sun, 40 % shade) and rainwater suppression (3 levels, full rainwater, November to March compared to the wet months and varied in parallel 1/3 rainwater suppression, 2/3 rainwater suppression) on pods and with soil moisture contents (ϴw). The values of ϴw ranged between 0.20 beans physical characteristics. The second group investigated the in- and 0.45 m3m− 3 among the treatments (Fig. 2). While overall ϴw was fluence of shade, rainwater suppression and day with either 6 levels higher under the shade compared to the sun, this depended on the soil (Sep-19, Dec-19, Feb-20, Apr-20, Jul-20, Sep-20) on gas exchange and depth, as differences were larger in deep soil layers (Fig. A.6). However, chlorophyll fluorescence; or 26 levels (Nov-2018, Dec-2018 up to Dec- 2/3 rainwater suppression plots in the full sun were moister for depths 2020) on water potential, stem expansion and litter fall. The third from 0 to 50 cm compared with the shade for reasons that we cannot group investigated the influence of shade, rainwater suppression, and account for. Generally, ѱw was high during predawn measurements and soil depth (13 levels, 0–10 cm, up to 120–130 cm) on soil moisture. The low at midday (Fig. A.7). Midday ѱw of the 2/3 rainwater suppression effects stated above were included as fixed effects together with their plots were - 0.7 MPa during the rainy season but reached values as low as interactions in a linear normal model. In addition to the fixed effects, the − 1.5 MPa in the dry season. statistical models also included random effects of plant id as well as temporal correlated residuals (for the second group) and spatial- 3.2. Photosynthesis temporal correlated residuals (for the third group) to model potential correlations between the observations. Thus, this resulted in linear Photosynthesis (Pn) was high in the wet months (July–September) mixed effects models, which were estimated using the nlme-package and tended to be highest in the full sun treatment. However, the effect of (Lindstrom and Bates, 1990) in the R statistical software (version shade depended significantly on the month of measurements with dif- 4.1.2, R Core Team, 2021). ferences between the shade and the sun being small in the dry months Conditions of homoscedasticity were verified by plotting residuals (Fig. 3, Table A.2). against predicted values, and the normality of residuals were validated Effects of rainwater suppression also depended significantly on the by normal quantile plots. When necessary, response variables were month of measurement, with the lowest values observed in the transformed to verify these conditions. Particularly, data from diurnal rainwater-suppressed treatments and differences increasing over time. measurements of water potential, transpiration, sub-stomatal CO2 con- Sub-stomatal CO2 concentrations (Ci) were high under shade especially centration, stomatal conductance, water use efficiency, stem expansion in February, April, and July 2020 and increased from full rainwater to 2/ and litter fall were log-transformed while soil moisture values were 3 rainwater suppression plots in both shade and full sun. square-root transformed. Moreover, for models with correlated re- Transpiration (E) was significantly higher under shade than in the siduals, the correlation structure was selected from a pool of potential full sun, but differences between rainwater suppression levels were not correlation structures via the Akaike Information Criteria (AIC). significant (Fig. 3, Table A.2). Values were between 1.5 and 5.5 mmol After the initial model selection and validation, the models were m− 2 s− 1 and increased under shade and in the wet months. This was reduced via the backward selection method (Pope and Webster, 1972), caused by stomatal conductance (gs) which was higher under shade than and the final models were used for reporting results. Predicted means in the full sun. Again, the effects of rainwater suppression levels were were separated with multiple comparisons using Tukey's Honestly Sig- not significant. Water use efficiency (WUE) showed significant in- nificant Differences (Tukey HSD). teractions between shade levels, rainwater suppression and months, and was higher in the full sun than in shade in the full rainwater and 1/3 3. Results rainwater suppression treatments in the relatively wet months of April and July 2020. 3.1. Environmental conditions, plant water potential and soil moisture Dark adapted chlorophyll fluorescence was affected by interactions between shade and rainwater suppression, and by the time of mea- Rainfall varied during the experiment, being more evenly distributed surement (Table A.2). Chlorophyll fluorescence was low during the dry during 2019 than in 2020. The annual rainfall was 1110 mm in 2019 and months of December and February 2020 (Fig. 3) in all the treatments 1250 mm in 2020. Still, both years had dry conditions around February and was very low in the full sun treatments compared with the shade and August, however, more pronounced in 2020. Photosynthetic active treatments. It decreased with increasing level of rainwater suppression, radiation (PAR) values at the experimental site also varied based on the indicating photoinhibition in these treatments. day of measurement (Fig. A.3). Although the shade nets were supposed to provide 40 % shade, measurements with the portable gas analyser 3.3. Litter fall, stem expansion and carbon accumulation suggested that reductions in PAR values were variable and on average slightly higher as values ranged between 34 and 58 % of the radiation Effects of shade on litter production depended on the level of rain- under full sun, depending on the month (Fig. A.4). Relative humidity water suppression and on the time of collection (Table A.3). In the dry under the nets was higher than in the full sun, corresponding to an season (November – February), litter production peaked and increased average increase of 4–11 % depending on the month. The corresponding in the full sun plots compared to the shade plots (Fig. 4). sub-canopy temperatures were on average 1.5–3.1 ◦C lower in shade Rainwater suppression increased litter fall, with the 2/3 rainwater 5 E.O. Mensah et al. S c i e n c e o f t h e T o t a l E n v i r o n m e n t 899 (2023) 165657 Fig. 2. Monthly variations of rainfall (blue bars), temperature (red line) and relative humidity (black line) measured from Nov. 18 - Dec. 2020 (A), volumetric soil moisture content (ϴw) measured from Aug. 2019 - Dec. 2020 (B) and predawn water potential measured from Nov. 2018 - Dec. 2020 (C) as affected by shade and water suppression levels. Soil moisture could not be measured earlier due to difficulties encountered with the moisture probe. Bars indicate standard error (n = 3). Dark background represents dry periods. 6 E.O. Mensah et al. S c i e n c e o f t h e T o t a l E n v i r o n m e n t 899 (2023) 165657 Fig. 3. Effects of shade and water suppression on cocoa photosynthesis (Pn), transpiration (E), stomatal conductance (gs), sub-stomatal CO2 concentration (Ci), water use efficiency (WUE) and chlorophyll fluorescence (Fv/Fm). Bars indicate standard error (n = 3), and stars indicate significant differences between shade and full sun (***adj P < 0.001, **adj P < 0.01, *adj P < 0.05). Dark background represents dry periods. suppression treatments in the full sun conditions giving the highest were between 3.9 and 6.1 mm year− 1 while monthly changes varied monthly litterfall of 1.2 Mg ha− 1 in February 2020 (Fig. 4A). Annual between − 1.0 to 2.5 mm month− 1. Expansion rates of plants in full litter fall in shade ranged between 3.6 and 6.2 Mg ha− 1 for the rainwater rainwater plots were on average 2.7 mm year− 1 higher than values in 1/ suppression levels while under the full sun conditions, litterfall was 4.4 3 rainwater suppression plots and 3.3 mm year− 1 higher than values in Mg ha− 1 for full rainwater plots and 6.7 Mg ha− 1 in 2/3 rainwater 2/3 rainwater suppression plots. On the other hand, values for the 1/3 suppression plots. rainwater suppression plots and the 2/3 rainwater suppression plots did High litter fall coincided with low canopy density, which showed not differ significantly. interactions between shade, rainwater suppression and month of Carbon accumulation was not affected significantly by the shade assessment. Values were generally high in full rainwater plots in shade levels, whereas the effects of rainwater suppression were only significant in the wet months but were low in the 2/3 rainwater suppression at 10 % (Table A.3). On average, 4.54 Mg C ha− 1 was accumulated by treatments and under the full sun (Fig. 4B). the 12-year-old cocoa plants before the start of the experiment. After Stem expansion was affected by rainwater suppression and month of almost three years of shade and rainwater suppression, carbon accu- measurement but not by shade (Table A.3), increasing at the start of the mulation increased by about 2.73 Mg C ha− 1 under shade and 2.33 Mg C wet season (between March to July) but declining towards the end of the ha− 1 under full sun conditions. Carbon accumulation was on average year for all treatments (Fig. 4C). In the dry months of January and 1.04 Mg C ha− 1 lower in the shade - 2/3 rainwater-suppressed plots than February 2020, growth almost stopped. Yearly total stem expansions in the full rainwater treatments, while under the full sun conditions, it 7 E.O. Mensah et al. S c i e n c e o f t h e T o t a l E n v i r o n m e n t 899 (2023) 165657 Fig. 4. Effect of different levels of shade and water suppression on litter fall (A), canopy density (B) and stem expansion assessed as diameter increase of cocoa (C) monitored for two years and three months. Data on litter fall were measured from Oct. 2018 – Dec. 2020; stem expansion from Dec. 2018 – Dec. 2020; and canopy density from Jan. 2019 – Dec 2020. Bars indicate standard error (n = 3). Dark background represents dry periods. 8 E.O. Mensah et al. S c i e n c e o f t h e T o t a l E n v i r o n m e n t 899 (2023) 165657 Fig. 5. Effects of shade and water suppression on annual average number of flowers (A), cherelles (B), aborted cherelles (C), pods, (D) and damaged pods (E) at 1.5 m of the cocoa trees. Means with different letters are statistically significant at P < 0.05 (Tukey's HSD). Number of pods, flowers and cherelles were assessed from 0.50 m to 1.5 m of the stem of the cocoa tree monthly from January 2019 to December 2020. Bars indicate standard error (n = 3). Table 1 Effects of shade and water suppression on pods and beans physical characteristics. Means are ± standard error (n = 3). Means in a row not sharing letters are significantly different at p < 0.05 according to Tukey's HSD. Shade levels Shade Sun Rainwater levels Full 1/3 rainwater 2/3 rainwater Full rainwater 1/3 rainwater 2/3 rainwater rainwater suppression suppression suppression suppression Pod physical appearance Pod weight (g pod− 1) 516 ± 122a 475 ± 151abc 486 ± 158ab 479 ± 104ab 455 ± 115bc 431 ± 117c Pod length (cm-pod− 1) 15.6 ± 1.6a 15.0 ± 1.2ab 15.2 ± 0.5ab 15.2 ± 1.7ab 15.1 ± 0.2ab 14.5 ± 0.4b Pod diameter (cm pod− 1) 8.5 ± 0.3a 8.2 ± 0.1b 8.2 ± 0.3b 8.1 ± 0.4b 8.0 ± 0.9b 8.1 ± 0.2b Length/Diameter 1.8 ± 0.2b 1.8 ± 0.2b 1.8 ± 0.2b 1.9 ± 0.1a 1.9 ± 0.2a 1.8 ± 0.2b Bean quantity and weight Beans/Pod 36.5 ± 1.2a 35.9 ± 2.2a 36.7 ± 3.7a 34.4 ± 5.6b 34.3 ± 2.6b 34.8 ± 3.6b Total bean weight (g 123.5 ± 113.8 ± 12.1abc 117.4 ± 9.1ab 114.9 ± 103.2 ± 15.2c 107.0 ± 18.2bc pod− 1) 14.7a 44.0abc % Beans weight/Pod 24.5 ± 4.1ab 24.6 ± 4.8ab 24.4 ± 3.8ab 23.7 ± 3.9ab 22.9 ± 3.6b 25.1 ± 4.2a Fresh weight (g bean− 1) 3.5 ± 0.4a 3.2 ± 0.1ab 2.8 ± 0.2c 3.0 ± 0.2bc 2.7 ± 0.5 cd 2.4 ± 0.2d Dry weight (g bean− 1) 1.3 ± 0.7a 1.2 ± 0.1ab 1.2 ± 0.1ab 1.3 ± 0.1ab 1.2 ± 0.1ab 1.1 ± 0.1b Moisture (g bean− 1) 2.2 ± 0.4a 1.9 ± 0.1ab 1.6 ± 0.1c 1.7 ± 0.1bc 1.5 ± 0.4 cd 1.3 ± 0.2d was about 0.61 Mg C ha− 1 lower compared with the full rainwater plots On the other hand, trees under rainwater suppression in both the shade (Table A.5). levels had low numbers of cherelles. Mean pod numbers varied between 7 and 20 tree− 1 year− 1 with plants under the shade producing more pods 3.4. Yield than plants under the full sun and lower numbers in the water- suppressed treatments (Fig. 5D). Pod numbers peaked during the wet The number of flowers was influenced by interactions between shade months (Fig. A.8). There were large differences among individual trees and rainwater suppression and was highest in the shaded full rainwater with pod counts ranging from 0 to 79 pods tree− 1 year− 1. The numbers plots, reaching 3000 tree− 1 year− 1 for the one-meter section of the stem of aborted cherelles and damaged pods were not significantly affected that was evaluated. Values were lowest in the full sun plots under 2/3 by the rainwater suppression levels but were significantly higher under rainwater suppression, where averages were ca. 1600 tree− 1 year− 1 the shade nets than under the full sun (Fig. 5C & E). (Table A.3, Fig. 5A). Average pod weight ranged between 431 g and 516 g among treat- Though the number of flowers was high, the number of cherelles was ments (Table 1), with pods from the shade being 20 to 55 g heavier than much low with values between 10 and 40 tree− 1 year− 1. Thus, only pods from the full sun conditions. about 2 % of the flowers developed into cherelles and only about 1 % Rainwater suppression reduced pod weight by about 10 % in the sun developed into mature pods (Fig. 5B & D). The shaded plants showed and 8 % in the shade. Also, pod length and diameter were negatively higher numbers of cherelles compared with the full sun plants (Fig. 5B). affected (Table 1). The average number of beans per pod varied between 9 E.O. Mensah et al. S c i e n c e o f t h e T o t a l E n v i r o n m e n t 899 (2023) 165657 Fig. 6. Effect of shade and water suppression on yield of cocoa plants between September 2018 and March 2021. Means with different letters are statistically significant at P < 0.05 (Tukey's HSD). Bars indicate standard error (n = 3). 34 and 37 with plants in the shade producing 2 to 4 beans more per pod conductance suggests a poor stomatal regulation in response to drought than plants in the sun. Hence, the total bean fresh weight per pod was in cocoa. Stomatal conductance (gs) was significantly affected by shade 103 g to 124 g for the shade trees receiving full rainwater, yielding levels but not by rainwater suppression levels, showing limited control almost 10 g more per pod than plants in the sun. Total bean fresh weight of water loss in cocoa (De Almeida and Valle, 2007). The relationship per pod was reduced by about 8 % in the shade and 10 % in the full sun between stomatal conductance and leaf water potential differs among as rainwater suppression increased from full rainwater to 2/3-rainwater groups of plants (Qaderi et al., 2019). It should be noted, however, that suppression. Similar tendencies were seen for fresh and dry weight per stomatal conductance was generally low at the four last assessments, to bean. some degree coinciding with periods of low precipitation. Carbon di- Dry bean yield (in kg ha− 1 season− 1) was significantly higher under oxide (CO2) concentrations inside the leaf increased with increasing the shade than in the sun, being 12 to 45 % higher at all levels of rainwater suppression despite the lack of differences in stomatal rainwater suppression (Table A. 4, Fig. 6). Rainwater suppression conductance, suggesting non-stomatal limitations to photosynthesis decreased yields to <50 % in the 2/3 rainwater suppression treatment, (Brodribb, 1996). At high-stress levels, impaired photosynthetic meta- compared to the full rainwater treatment. Yield was generally low in the bolism may be caused by weakening of photosystem II and alteration of minor seasons with averages between 87 and 293 kg ha− 1season− 1 but the thylakoid membrane proteins (Marino et al., 2018). was much higher in the major season ranging from 286 to 1105 kg Shade improved microclimatic conditions reducing average air ha− 1season− 1. Differences were especially pronounced during the 2020 temperatures and maximum temperatures compared to the full sun major season. Analysing the seasons individually, differences between plots, while relative humidity was higher. Plants under full sun were treatments were non-significant for the 2018 major season (while the exposed to high solar radiation combined with high temperatures. In the treatments were not yet fully installed) and the minor seasons in 2019 dry months of March and April, below canopy temperatures were as high and in 2020, but significant for the major seasons in 2019 and in 2020. as 42 ◦C, values above the reported optimum for growth of 24 ◦C - 34 ◦C (Gomes and Kozlowski, 1987; Najihah et al., 2018) and for photosyn- 4. Discussion thesis of 31 to 35 ◦C (Balasimha et al., 1991; Yapp, 1992; Mensah et al., 2022). Though reported cases show cocoa plants surviving at 40 ◦C To our best knowledge, this is the first experiment to investigate the (Valle et al., 1990), physiological activities of key elements of photo- combined effects of shade and limitations in water supply under field synthesis, including PSII activation, ATPase activity and the carbon conditions in mature cocoa trees. Our setup with shade nets and plastic assimilation process, are impaired (Mathur et al., 2010; Chen et al., panels resulted in clear differences in light levels, soil water contents and 2012; Carrion-Tacuri et al., 2013). Hence shade, through the reduction water status of the trees, and cocoa plants responded by changes in of temperatures, may reduce the risks of high temperatures. The evi- physiology, growth, and yield. However, as we will discuss below, the dence of large differences in soil moisture content between shade and absence of interactions between shade and rainwater suppression full sun in deep soil layers might be due to high relative humidity under treatments for important characters did not support our hypothesis that shade resulting in reduced evapotranspiration and facilitating water shade would fully compensate for the negative effects of drought. retention at the deep soil layers. This would be an advantage under Even though levels of drought stress were not lethal, trees were shade, conserving soil moisture for use during dry periods. negatively affected by drought, having decreased growth rates, larger At the same time, solar radiation for full sun conditions was high leaf fall, thin foliation, and a possible decrease in biomass accumulation. with PAR ranging between 1200 and 2000 μmol m− 2 s− 1, much above The low leaf water potentials in rainwater-suppressed plants reduced the light saturation point of 300 to 550 μmol m− 2 s− 1 for cocoa (Avila- photosynthesis and led to photoinhibition as indicated by the low values Lovera et al., 2016; Salazar et al., 2018; Mensah et al., 2022). This is of Fv/Fm, commonly seen in drought-stressed plants (Janusz et al., 2006; another likely cause for the photoinhibition that was indicated by the Bae et al., 2008; Moser et al., 2010; De Almeida et al., 2016). low Fv/Fm values. Values averaging between 0.65 and 0.77 have been The absence of effects of rainwater suppression on stomatal reported in full sun cocoa plantations (Galyuon et al., 1996; Bae et al., 10 E.O. Mensah et al. S c i e n c e o f t h e T o t a l E n v i r o n m e n t 899 (2023) 165657 2008) but values of 0.8 noted under shade showed intact PSII systems Niether et al., 2020) where higher yields were observed under full sun (Acheampong et al., 2013; De Araujo et al., 2017). Still, the plants in full than in agroforestry conditions. The question is whether our results can sun conditions were able to maintain higher photosynthetic rates per be translated directly to agroforestry. This study applied shade nets to unit area compared to trees under shade, indicating that photosynthesis provide uniform shade, but due to high costs, this is not an affordable was limited by light under shade. This seems to have been compensated shade management practice for many farmers. The alternative will be to for by the lower leaf fall and high canopy density under shade. A higher apply natural shade from shade trees extending above the canopy of leaf area with high PSII activity may have contributed to higher gross cocoa. There is an increasing body of evidence showing that shade trees canopy photosynthesis under shade compared to full sun, in turn leading may increase cocoa yields under conditions of low agricultural inputs to higher rates of pods formation and better development of pods under (including fertilizers and pesticides) (Wouter et al., 2016; Andres et al., shade. Unlike plants under shade, photoinhibition experienced by the 2018; Sauvadet et al., 2019; Asare et al., 2019; Asitoakor et al., 2022). plants under full sun may have shortened leaves' life span and increased However, although such trees provide shade that will benefit the cocoa litter fall, resulting in lower or reduced gross canopy photosynthesis trees, they may also compete with cocoa for water and nutrients, as well though individual leaf photosynthesis was high. as influencing the occurrence of pests and diseases (Blaser et al., 2018; Dry bean yield was increased under shade in comparison to the full Mortimer et al., 2018; Kaba et al., 2020;). Abdulai et al. (2018) showed sun. Although the abortion of flowers and cherelles was higher in shade that shade trees could have a negative impact on cocoa under severe than in the full sun, the fact that the numbers were higher from the drought stress conditions, and that such interactions depended on the beginning means that number of pods ended up being higher. <2 % of shade tree species. There is a need to investigate how cocoa physiology the flowers produced developed into cherelles among all the treatments, and performance are influenced by water stress when under agroforestry thus confirming previous studies (de Almeida and Valle, 2007; Groe- conditions, and in particular, how they are influenced by various tree neveld et al., 2010; Carr and Lockwood, 2011). Though flower abortion species in differing local conditions. and cherelle wilt may be inherent traits to manage resource allocation (Mckelvie, 1956; Handley, 2016), below cocoa canopy temperature in 5. Conclusion the full sun conditions were high which may have affected flower development to cherelles, especially in the water-suppressed plots. Overall, the experiment confirmed that shade has a positive impact Stigma viability, pollination, pollen tube growth and early embryo on cocoa, not only enhancing yield but also the apparent health and development are vulnerable to heat stress (Giorno et al., 2013; Lamaoui growth of the cocoa trees. As expected, rainwater suppression led to et al., 2018). Lack of rainwater during anthesis and early cherelle drought and decreased performance of the cocoa trees in terms of development also cause abnormalities in floral organs, interfering with physiological performances, growth, and yield. However, our expecta- pollination and inducing abscission of newly formed embryos (Saini, tion that shade would remedy the consequences of the drought was not 1997). In effect, Frimpong-Anin et al. (2014) observed a larger drop of unequivocally confirmed, as there were only a few interactions between unpollinated flowers in the dry season than in the rainy season. Pod shade and rainwater suppression, suggesting that the effects of the two damage in our study was, however, more pronounced under the shade factors were mainly additive. This means that even though shade will than under the full sun contrary to previous studies (Ofori-Frimpong benefit the cocoa plants, it will not prevent them from being stressed by et al., 2007). Bos et al. (2006) observed that early and pathogenic fruit low soil water availability. Further research is needed to clarify how losses were more numerous under shade. Low temperature combined agroforestry shade tree species impact cocoa under drought, particularly with increased humidity under shade could have provided a favourable regarding their root profile and ability to tap water at lower soil depths environment for fungal diseases such as Phytophthora spp. causing and enhancing water availability in the upper soil layers via hydraulic damage to cherelles and pods (Delgado-Ospina et al., 2021). Still, the lift. higher initial numbers of flowers, the heavier pods and beans under the shade compared to the full sun conditions resulted in an overall higher Funding yield under shade. Additionally, pruning of cocoa trees may provide a more uniform light distribution within the canopy and allow better This study was funded by the Ministry of Foreign Affairs of Denmark airflow, thus reducing moisture that could otherwise favour fungal (DANIDA) through the Climate Smart Cocoa Systems for Ghana development (Riedel et al., 2019; Delgado-Ospina et al., 2021). (CLIMCOCOA) [grant number 16-P02-GHA]. Yield was sensitive to water availability and declined at increasing rainwater suppression, and bean quality declined in response to limited CRediT authorship contribution statement soil moisture. Similar studies of yield response to water availability have been reported by Abdulai et al. (2018) in West Africa, Gateau-Rey et al. Eric Opoku Mensah: methodology, investigation, data collection, (2018) in South America and Wuriandani et al. (2018) in Asia. In- writing-original draft, formal analysis, Anders Ræbild: conceptualiza- teractions between shade level and rainwater suppression level were tion, supervision, validation, methodology, writing-reviewing and significant for some of the variables, including soil water content, editing, Richard Asare: conceptualization, resources, supervision, diurnal variations in water potential, WUE and Fv/Fm, mostly suggesting writing-reviewing and editing, Christiana A. Amoatey: supervision, that effects of water stress were less pronounced under shade compared project administration, writing- reviewing and editing, Bo Markussen: to full sun. This also appeared to be the case for canopy density, number visualization, validation, formal analysis, Kwadwo Owusu: resources, of flowers and parameters related to pod dimensions and number of funding acquisition, project administration, Bismark Kwesi Asitoakor: seeds. However, for variables such as photosynthesis, substomatal CO2 investigation, data collection, writing-reviewing and editing, Philippe concentration, predawn water potential, and most importantly the yield, Vaast: conceptualization, supervision, validation, methodology, interactions were not significant despite clear and significant effects of writing-review and editing both rainwater suppression and shade level. Hence the effects of stress on these parameters are mainly additive. In contrast to our hypothesis, Declaration of competing interest this leads to the interpretation that shade may not prevent cocoa yield from declining under drought stress. Thus, the overall better perfor- The authors declare no conflict of interest. mance of cocoa under shade can only partly compensate for the reduced yield during drought episodes. Data availability In the present study, yield increased under shade in contrast with some previous reports (Ahenkorah et al., 1974; Blaser et al., 2018; Data will be made available on request. 11 E.O. Mensah et al. S c i e n c e o f t h e T o t a l E n v i r o n m e n t 899 (2023) 165657 Acknowledgement stresses. Plant Physiol. Biochem. 46, 174–188. https://doi.org/10.1016/j. plaphy.2007.10.014. Balasimha, D., Daniel, E.V., Bhat, G., 1991. Influence of environmental factors on We acknowledge Noah Adjei Owusu for assisting with data collec- photosynthesis in cocoa trees. Agric. For. Meteorol. 55, 15–21. https://doi.org/ tion, Nana Francis K. Gyabeng (Oluu) for offering his farm for the 10.1016/0168-1923(91)90019-M. research, the people of Sefwi Kunuma (Mile 82) and other field workers Baligar, V.C., Bunce, J.A., Machado, R.C.R., Elson, M.K., 2008. 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