Effects of canopy species over Theobroma grandiflorum in agroforestry systems in the Brazilian Amazon

Efeitos de espécies de dossel em Theobroma grandiflorum em sistemas agroflorestais na Amazônia brasileira

Abstract:

Theobroma grandiflorumis particularly suitable for agroforestry systems (AFSs). However, to design stable, reliable and profitable AFSs, it is necessary to define which canopy species best interact with T. grandiflorum. This study compares two AFSs established, as participatory research, on rural properties in the municipality of Tomé Açu, Pará State, Brazil, monitored from 2005 to 2019.Along with crop species cultivated in the initial phase, Swietenia macrophylla and Khaya grandifoliola were used as canopy species. Fruit production and survivalrate of T. grandiflorum were evaluated at four distance levels from the canopytrees. We also measured the development of both canopy species to estimate growth rates,wood, and aboveground biomass (AGB) production potential. K.grandifoliola had the effect of reducing production and survival rates of T. grandiflorum in AFSs,while S. macrophylla best met the required criteria to keep the AFS viable for fruit production. However, as a timber species, K. grandifoliola presented better responses in terms of vigor, AGB and wood production than S. macrophylla, and therefore offers a viable alternative to the use of the native species. Thus,despite the biological results achieved for T. grandiflorum production, thechoice of canopy species to be included in the AFSs must also consider the goals of eachfarmer.

Index terms
Cultivation systems;; Swietenia macrophylla;; Khaya grandifoliola;; Competition

Resumo:

Theobroma grandiflorum é particularmente adequado para sistemas agroflorestais (SAFs). Entretanto, para projetar SAFs estáveis, confiáveis rentáveis,é necessário definir quais espécies de dossel melhor interagem com T.grandiflorum.Este estudo analisa dois SAFs para comparar suas antagens diferenciais. Os SAFs foram implantados, como pesquisa participativa, em propriedades rurais do município de Tomé-Açu, Pará, Brasil, e foram monitorados de 2005 a 2019. Junto com as espécies de sub-dossel cultivadas na fase inicial, foram utilizadas Swietenia macrophylla e Khaya grandifoliola como espécies de dossel. A produção defrutos e a taxa de sobrevivência de T. grandiflorum foram avaliadas em quatro níveis dedistância da copa das árvores. Também medimos o desenvolvimento de ambas as espécies de dossel para estimar as taxas de crescimento, o potencial de produção de madeira e biomassa acima do solo (AGB). K. grandifoliola teve o efeito de reduzir a produção e as taxas de sobrevivência de T. grandiflorum em SAFs, enquanto S. macrophylla atendeumelhor aos critérios exigidos para manter o SAF viável para produção de frutos. Contudo,como espécie madeireira, K. grandifoliola apresentou melhores respostas em termosde vigor, AGB e produção de madeira do que S. macrophylla, e, portanto, oferece uma alternativa viável ao uso da espécie nativa. Assim, apesar dos resultados biológicos alcançados para a produção de T.grandiflorum, a escolha das espécies de dossel a seremincluídas nos SAFs também deve considerar os objetivos de cada agricultor.

Termos para indexação
Sistemas de cultivo;; Swietenia macrophylla;; Khaya grandifoliola;; Competição

Introduction

Agroforestry systems (AFSs) are land-use models that promote simultaneous or sequential interaction among crop and canopy species. They are important alternatives to conventional models used in tropical environments, such as monoculture (UTOMO et al. 2016) and swidden or shifting cultivation systems (VASHUM; JAYAKUMAR 2016).

AFSs are effective in intensifying land use as several species that would normally occupy different areas in a landscape are planted together (TORRALBA et al. 2016). Because perennial species are commonly used, AFSs also offer to rural producers the economic benefits of diversified and staggered financial returns over time. It is important to stress that when planning an AFS, the choice of species must consider economic factors such as the target consumer market, as well as agricultural inputs and the key species selected for the system, which may determine its density, and biological factors, like characteristics of adaptation and interaction between species.

AFSs are common in the Amazon region and generally occur in the form of agroforestry orchards, a subsistence model based on local peoples’ traditional knowledge (CASTRO et al. 2009). In the Northeast of Pará State, Brazil, particularly in Tomé Açu municipality and surroundings, commercial AFSs are popular and appeared in the late 1960s as an adaptation of traditional cultivations by descendants of Japanese settlers in response to phytosanitary problems with monoculture crops of Piper nigrum L. Some of the most used species in AFSs include Swietenia macrophylla King and Theobroma grandiflorum (Willd. ex. Spreng.) Schum.Khaya grandifoliola A. Juss is also widely used in AFSs as well as recommended by professionals in the region.

Swietenia macrophylla, of the Meliaceae family, is a large tree native to the Amazonian regions of Brazil, Peru, and Bolivia. It can reach 70 m in height and 3.5 m in diameter.

Its wood has excellent mechanical properties and is highly valuable in the international market. As such, the species has been indiscriminately exploited, resulting in the loss of 95% of adult individuals in primary forests (FREE et al. 2014). It is currently listed as an endangered species in appendix II of the Convention on International Trade in Endangered Species (CITES) (GROGAN; LOVELESS, 2013). Khaya grandifoliola, also from the Meliaceae family, is native to the West Coast of Africa (VERZIGNASSI et al.2009) and was introduced into Brazil. It has similar wood properties to S. macrophylla, is resistant to attacks by the borer moth Hypsipyla grandella and currently has no legal restrictions on harvesting (FRANÇA 2016). Theobroma grandiflorum, of the Malvaceae family, produces fruits whose pulp and almonds are used in the manufacture of food, pharmaceuticals and cosmetics (ALVES et al. 2020).

With the use of morphometric and biomass analysis it is possible to assess the level of inter- and intraspecific competition among tree species of the upper stratum in an AFS, which may interfere in the luminosity reaching lower strata, as well as the water and nutrients availability (ROMAN et al.2009).

Such aspects support decision-making about the management of each system’s component, whether agronomic or silvicultural, considering both their biological and economic viability (PEZZOPANE et al., 2024). Therefore, the goals of this study were to evaluate the influence of two canopy species on the development, production, and survival of the fruit species T. grandiflorum, and assess the growth of canopy species.

Material and Methods

The study was conducted from 2005 to 2019 in the municipality of Tomé Açu, Northeast Pará state, 120 km from the state capital, Belém, Brazil.

The municipality is a pioneer in the use of commercial AFS in the Brazilian Amazon due to the influence of an agricultural cooperative created by Japanese Brazilian farmers, which processes and distributes products from these systems. The experiments were carried out in two different AFSs, located on two rural properties, in a participative approach.

The farmers were responsible to maintain the experiment, following the guidelines previously established by the research team, making the research results readily visible and accessible to local producers.

According to the Köppen classification, the climate of the region is Ami, with an average annual temperature of 26.3 °C, precipitation of 2,746 mm, and relative humidity of 85.3%.

The soil in both experimental areas is deep and well-drained and classified as Oxisol with medium texture, low fertility, low organic matter content, and high acidity.

Initially, the field where AFS 1 was installed was cultivated with Piper nigrum for seven years, followed by an intercropping of Capsicum chinense Jacq., Carica papaya L., and Curcubita spp. during five years, followed by a fallow period of 10 years.

Subsequently, in the last 14 years, the area was used for the agroforestry system studied herein. AFS 2 was established on a property 15 km away from the previous one. The area was initially cultivated with P. nigrum (10 years), then went through a fallow period (12 years) and, in the last 14 years, was occupied by the experiment presented in this study. The preparation of the experimental areas consisted in the vegetation removal from the fallow period and the application of one ton of dolomitic limestone per hectare.

The specific characteristics of each experimental area are described below: AFS 1: consisted of Theobroma grandiflorum with a spacing of 5 x 5 m (density = 400 plants/ha); Passiflora edulis, which remained in the area for only three years, with a spacing of 5 x 2.5 m (800 plants/ha); and Swietenia macrophylla with a spacing of 20 x 10 m (50 plants/ha). It is located under the coordinates 02º 26’ 03” S and 48º 18’ 37” W.

AFS 2: Theobroma grandiflorum with a spacing of 6 x 4 m (416 plants/ha); Musa spp., with a spacing of 6 x 4 m (416 plants/ ha), removed from the area after the fifth year; P. nigrum with a double spacing of 2 x 2 m, and 4 m between double rows (1600 plants/ha), ending its cycle in the seventh year; and Khaya grandifoliola at a spacing of 18 x 10 m (55 plants/ha). The tested systems were samples of the commercial AFSs adopted in the region, including the crop species.

The geographical coordinates of this AFS are 02º 32’ 54” S and 48º 15’ 54” W.The recommended fertilization for T. grandiflorum, after the plants reached production stability from the eighth year after implementation, was 1.0 kg/plant of the formula 10-28-20, which corresponds to 40 kg of N, 112 kg of P and 80 kg of K, per hectare, applied at the beginning and the end of the rainy season. Additionally, 20 kg/ha of FTE and 120 kg/ha of dolomitic limestone were applied at the end of the rainy season.

To test the effects of canopy trees over T.grandiflorum plants, which can be induced by competition above and below the soil, four distance levels in each experiment were established between canopy trees and T.grandiflorum individuals (Figure 1). In AFS 1,each tested distance was composed of four plants of T. grandiflorum, thus 16 plants were measured concerning each S. macrophylla tree, for a total of 320 T. grandiflorum plants and 20 S. macrophylla trees (Figure 1A).

Figure 1
Schematic diagram of distance levels between Theobroma grandiflorum and the canopy species Swietenia macrophylla (A) and Khaya grandifoliola (B) in two experimental agroforestry systems in the municipality of Tomé Açu, Pará, Brazil. Level 1: 2.3 m from S. macrophylla to T. grandiflorum and 3.6 m from K. grandifoliola to T. grandiflorum; Level 2: 5.5 m from S. macrophyllato T. grandiflorum and 6.7 m from K. grandifoliola to T. grandiflorum; Level 3: 7.3 m from S. macrophylla to T. grandiflorum and 9.2 m and K. grandifoliola to T. grandiflorum; Level 4: 8.8 m from S.macrophylla to T. grandiflorum and 13.4 m and K. grandifoliola to T. grandiflorum.

In AFS 2, four plants also formed at each distance level, so that 16 plants of T. grandiflorum were measured concerning each K. grandifoliola tree.

We sampled 144 plants of T. grandiflorum and nine individuals of K.grandifoliola, following the proportion 4:1(Figure 1B).

When installing the AFS, the species were planted simultaneously. At the end of the productive period of the short-cycle species (P. edulis, Musa spp., and P. nigrum), T.grandiflorum remained in consortium only with the canopy species. This configuration began in the third year after planting and continued until the 14th year of evaluation.

The following response variables were used to assess the responses of T. grandiflorum: number of fruits and average weight of fruits, which were used to estimate fruit production (kg/plant/crop) based on the series of 11 harvests. T. grandiflorum survival throughout the years was also assessed.

In the second year after the AFSs establishment, we began collecting data on tree species, measuring total height (Ht) and diameter at breast height (DBH; 1.3 m from ground level). The commercial height (Hcom) was collected in the last year of evaluation. In the first years of monitoring, the height was measured using a metric ruler and later with a digital hypsometer, model VERTEX IV. DBH was estimated from the circumference at breast height measured with a measuring tape and transformed to DBH.

Beginning in the fifth year after establishment, the crown diameter (CD) of the two canopy species was also measured. All data was collected annually at the plant level.

The commercial wood volume was estimated through the equation: CWV = -9.38450 + 2.06586 x ln(DBH) + 0.72929 x ln(Hcom), as proposed by Fernandes et al. (2017) for S. macrophylla in a silvopastoral system; and the cylinder volume x form factor (0.5) method for K. grandifoliola.

Some canopy-related parameters were estimated, such as crown projection area (CA = (CD²π)/4), slenderness degree (Ht/DBH), index of protuberance (CD/DBH), and index of enclosure (CD/Ht). From height and DBH, we estimated the aboveground biomass (AGB) of each canopy species through the general allometric equation: AGB = 0.0673(ρDBH² H)^0.976, where ρ is the wood density, in g cm^-3 (CHAVE et al. 2014). The wood density of each species was obtained from Global Wood Density Database, using the BIOMASS package, at R software (CHAVE et al. 2009, RÉJOU‐MÉCHAIN et al.2017, R CORE TEAM, 2021). We considered ρ = 0.462 for K. grandifoliola, and ρ = 0.63 for S. macrophylla.

Theobroma grandiflorum production data were analyzed through an analysis of variance (ANOVA), after complying with its assumptions, considering a repeated measures design using levels as categorical variables and canopy species’ AGB as a covariate.

Subsequently, an additive regression model (AALEN, 1993) was fitted to analyze the survival data throughout the evaluation years, accounting for the AGB as a time-dependent covariate.

All the analyses were performed in the R software, using the packages “Survival” (THERNEAU, 2021) and “Survminer” (KASSAMBARA et al. 2021) for the survival analysis. Although it was not possible to perform statistical comparisons between the canopy species, the average values of the measured and estimated variables were calculated to draw a parallel between their performances over the years of evaluation.

Results and Discussion

Performance of canopy species

In AFSs, canopy species are planted at a wider spacing than in single-species plantations, which generates less intra- and interspecific competition in the initial years (FLETCHER et al., 2012).

In the current experiment, this condition allowed the species to grow optimally in the first years after the experiment began. For Khaya grandifoliola, Soranso et al. (2016) found a positive correlation between increases in growth rate and the spacing adopted, demonstrating that thinning decreases intraspecific competition, which is reflected in radial increases of the wood.

Khaya grandifoliola presented highest growth estimates (Figure 2). On average, K. grandifoliola grew 3.5 m in height and 5.5 cm in diameter per year in the first four years of the experiment. Swietenia macrophylla grew 2.0 m in height and 3.5 cm in diameter in the same period.

After the initial period, there was a deceleration in tree growth. For K. grandifoliolathis deceleration occurred later, showing the optimal adaptation of this species to local AFS growing conditions. In the 14th year after the implementation of the AFSs, there were substantial differences concerning the canopy species growth. The total height was greater for K. grandifoliola, presenting values 30% higher than S. macrophylla (Figure 2). This influenced the commercial height, in which K. grandifoliola was 38% greater, on average, than S. macrophylla (Figure 2).

Figure 2
Evolution of growth (total and commercial height, diameter at breast height and commercial volume), morphometry traits (canopy projection area, slenderness degree, index of protuberance and index of enclosure) and aboveground biomass of the canopy species Swietenia macrophylla and Khaya grandifoliola over 14 years of cultivation in agroforestry system conditions in the municipality of Tomé Açu, Pará, Brazil.

Concerning DBH, K. grandifoliola also presented better performance than S. macrophylla (Figure 2). For estimated commercial wood volume, K. grandifoliola presented values almost 75% greater than S. macrophylla, reflecting the results obtained for height and DBH (Figure 2).

Worldwide, studies on K. grandifoliola showed that the species develops vigorously, both in height and diameter. Carmona et al. (2018), evaluating 16-year-old individuals in AFSs in Monte Alegre, Pará, Brazil, found lower values than the present study: 16.8 m in total height; 6.8 m in commercial height; and 30 cm in DBH.

These differences can be explained by wider spacing used in our study, in addition to soil and climate factors and the management of the species at the local level. Results found in the present study show that Swietenia macrophylla, even with a slower growth rate than K.grandifoliola, still presents average values for total height and DBH that are greater than those normally reported in literature.

Considering an ideal cutting age of approximately 15 years for Khayaspp., the trees measured in this study were close to the ideal harvest age. Oliveira et al. (2018), studying K. ivorensis trees with a 12 x 12 m spacing in Santo Antônio do Tauá, Pará, found an average volume of 1.31 m³/ plant, which is slightly lower than the average found herein. This demonstrates that the K. grandifoliola individuals analyzed in this study show normal development for the soil and climate conditions of Northeastern Pará.

In commercial terms, these results indicate that the replacement of one species by the other will provide a considerable increase in wood production, which would be reflected in greater economic returns. Considering the current and corrected prices through the Brazilian inflation of Roundwood (ITTO 2017; ITTO 2021), the financial returns of K. grandifoliola and S. macrophylla in the study AFSs would be 22,749.65 USD/ha and 4,134.00 USD/ha, respectively.

The revenues with production of T. grandiflorum fruits in 12 harvests would sum up 11,677.12 USD/ ha and 18,403.40 USD/ha with K. grandifoliola and S. macrophylla, respectively. The total gross revenue can reach 34,426.77 USD/ ha and 22,537.40 USD/ha. Considering a discount rate of 50% in establishment and maintenance costs of the orchards (SANTOS et al. 2020), the net revenue can reach up to 17,213.38 USD/ha and 11,268.70 USD/ha,respectively.

Given the results, K. grandifoliola seems to be the best recommendation for AFSs in the Amazon region, as it offers greater financial returns. Nevertheless, caution is needed before making decisions of this nature.

Because the system is a consortium of plants occupying different strata, it is fundamental to understand how canopy species affect shading levels. As such, analyzing aspects of the trees’ canopies is fundamental to assess this relationship (CARMONA et al.2018).

In terms of crown morphometry, K. grandifoliola had the greatest canopy projection (Figure 2). The slenderness degree of S. macrophylla was higher than K. grandifoliola, indicating less stability of the tree (Figure 2). The index of protuberance was similar among the two Meliaceae (Figure 2). K. grandifoliola obtained a high value for the index of enclosure, reflecting a wide crown distribution (Figure 2). Anglaaere et al. (2011) emphasize that species of the genus Khaya have dense and wide canopies which create high levels of shading.

The above-mentioned results are important indicators not only on the vegetative development of the canopy species but also on the level of competition they can exert over T. grandiflorum. However, a more robust parameter is the aboveground biomass (AGB) produced by each species (Figure 2). As expected, the AGB production of K. grandifoliola was considerably higher than S. macrophylla since the first measure, in the third year after the experiment beginning (first T.grandiflorum harvest). Comparatively, in the 14^th year (the last evaluation), S. macrophylla presented the same AGB production that K. grandifoliola had in the 6^th year of the experiment.

Opuni-Frimpong et al. (2013)and Warnasooriya and Sivananthawerl (2016) report the great capacity of Khaya species, particularly K. senegalensis and K. grandifoliola, to produce biomass both aboveground and belowground. This is reflected in the intensification of competition for light, water and nutrients throughout the system, causing high mortality rates and low production levels of shaded species, as observed herein and attested by the analyses.

On the other hand, if we consider the crown projection area of S. macrophylla, the species seems to promote lower levels of competition.

S. macrophylla does not project the canopy over a large area and has good growth in height, both aspects facilitate the penetration of light into the system and mitigate the negative effects resulting from the shading of the lower strata plants.

This can be related to the good levels of Theobroma grandiflorum productivity in this AFS, although other variables like competition for water and nutrients can also have effects on it.

The AGB production of S. macrophylla is substantially smaller than K. grandifoliola, probably due to its slower growth and smaller size, which contributes to the lower rates of competition. A lower biomass production indicates a lower transformation of raw materials, such as light, water, and nutrients, which will be available to species of the lower stratum. However, it is noteworthy that, despite being smaller, competition between S. macrophylla and T.grandiflorum is not null.

Relations of Theobroma grandiflorum with long-cycle canopy species

Using average values of T. grandiflorum in the AFSs as an indication of the area’s uniformity, there was little variation in vegetative development and fruit production in the first harvests. These results evidence that environmental conditions such as small soil variations, fertilizer residues from companion species, and cultural management had no effect on the initial development T. grandiflorum (Figure 3). As expected, the analysis determined that the effects of AGB, distance levels, and years have effect on the fruit production of T. grandiflorum (Table 1). For S. macrophylla, there was also a differential expression of year and AGB effects on plants present at different levels, a fact verified through the significance of the interactions.

This result is a robust indicator of competition between species.

Table 1
Mean squares and respective significances of the aboveground biomass (AGB), distance level, and year, and their interactions.

	Khaya grandifoliola	Swietenia macrophylla
AGB	1256.96*	134591*
Level	322.48*	950*
Year	3080.69*	16247*
Level x AGB	60.06ns	634*
Level x Year	130.6ns	223*

• ^*
  * and ^ns: Significant and non-significant differences, respectively, detected by Snedecor’s F test at 5% probability.

In the first five harvests, plants from both systems had similar production trends, with growth and fluctuation as expected for the crop, with no significant difference between distance levels (Figure 3).

From the sixth harvest onwards the systems differ substantially, with a tendency to increase yield in the intercropping with S. macrophylla (Figure 3A) and decrease yield in the intercropping with K. grandifoliola (Figure 3B).

The decrease of T. grandiflorum plants intercropped with K.grandifoliola occurred when the canopy species’ biomass had great increase.

The average production in the last five harvests (stable phase) showed a clear distinction in terms of the influence of canopy species on the T. grandiflorum performance. The most favourable was S. macrophylla, as it enabled greater fruit production at all distance levels. K. grandifoliola caused the greatest decrease in production in the T. grandiflorum production. Longer distances (levels 3 and 4) from T. grandiflorum resulted in better fruit production. This pattern was stronger in the S. macrophylla intercropping, since the competition against K. grandifoliola was spread over all distance levels.

Figure 3
Average (± standard error) of Theobroma grandiflorum fruit production in two agroforestry systems under two canopy species: Swietenia macrophylla (A) and Khaya grandifoliola (B), throughout 11 harvests, at four distance levels (nearest = 1, most distant = 4), in Tomé Açu, Pará, Brazil.

In the survival analysis, the aboveground biomass comes as a major factor, as well as the distance of T. grandiflorum plants in relation to canopy species. The AFS with S. macrophylla presented the highest survival rate, indicating less competition between the canopy and agronomic species(Figure 4A).

On the other hand, AFS with K. grandifoliola had lower survival rate, reaching less than 50% for levels 1, 2, and 3, in the last year of evaluation (Figure 4B).

Figure 4
Theobroma grandiflorum survival rate in two agroforestry systems with different canopy species: Swietenia macrophylla (A) and Khaya grandifoliola (B), throughout 11 years, at four distance levels (nearest = 1, most distant = 4), in Tomé Açu, Pará, Brazil. The coloured areas above and below the lines represent the levels’ standard errors.

Clearly, competition factors have influenced the different responses of T. grandiflorum both in terms of production and survival.

T. grandiflorum is a species native to the Amazon region that commonly occurs with S. macrophylla (ALVES et al. 2013; DEGEN et al. 2013); as such, they probably have adapted for mutual coexistence. Moreover, S. macrophylla has a more compact growth than K. grandifoliola, as observed in the present study, which reflects in the lower biomass production, and therefore can temper interspecific competition.

Despite producing less AGB per plant, S. macrophylla can bring negative effects on the T.grandiflorum fruit production and survival,according to the distance level. The exotic species in this study, K. grandifoliola, had the most negative impact on the performance of T. grandiflorum.

The species is well adapted to Amazonian conditions, with rapid and vigorous growth, and it can promote intense competition below-ground for water and nutrients and above-ground for light.

Conversely, if the main objective of an AFS is timber harvesting, such as for hardwood production, T. grandiflorum and other initially planted species can help to offset the planting and maintenance costs, at least in the first 10 years.

Santos et al. (2020),assessing an AFS in the same region, estimated a cost-benefit relation of 1.98 for T. grandiflorum, indicating its medium- and long-term financial viability.

As such, even if these species later die or are removed due to low levels of production, their inclusion in the system is justified. For this reason, the management of plant density and spacing is dependent on the objectives of the system and are equally as important as the choice of species.

Conclusion

The exotic species K. grandifoliola has shown good adaptation to the soil and climate conditions in Tomé-Açu, Northeastern Pará and, consequently, better responses in terms of vigour, AGB, and wood production than S. macrophylla.

On the other hand, S.macrophylla showed limited interference in the performance of the fruit tree T. grandiflorum under AFS conditions. K. grandifoliola harmed the production and increased mortality of T. grandiflorum.

Thus, when the focus of a system is on wood commercialization and the species of the lower strata are a means to offset costs, K. grandifoliolawould be the best option. Otherwise, the planting of the exotic Meliaceae should be done with caution, using larger planting spacing, fertilization, and irrigation in the dry period, mainly for the consortium crop species.

Data Availability

The data that support the findings of this study are available from the corresponding author, Alves, R.M., upon reasonable request.

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Edited by

• Scientific Editor
  Alexandre Pio Viana

• Associate Editor
  Gabriel Barbosa da Silva Junior

Publication Dates

• Publication in this collection
  08 Dec 2025
• Date of issue
  2025

History

• Published
  17 Nov 2025
• Received
  22 Aug 2024
• Accepted
  22 Sept 2025