Assessing the Susceptibility and Tolerance of Oil Palm Cultivars to Leaf-Bending: A Comparative Physiological and Nutritional Balance Study

Abstract

Selecting the best oil palm cultivars adapted to specific agro-climatic conditions helps ensure fruit and oil production success. Many biotic and abiotic problems can limit the productivity of the crop, some of which have not yet been described, as well as their symptoms and degree of impact. In oil palm, a disturbance known as leaf-bending occurs, in which the palms present a bending or breakage of the petiole in the leaves, representing a significant challenge for oil palm cultivation. Although leaf-bending in oil palm plantations is known, its effect on the palm’s performance and its possible causes are unknown. Thus, the objectives of the present work were to describe and propose a quantitative way to evaluate leaf-bending in different cultivars (Elaeis guineensis Jacq. and the interspecific O×G hybrid) and to evaluate the disturbance effect on the physiology and nutritional balance of the oil palm. The results showed that most leaves from leaf rings three and four of the palm phyllotaxis have the highest affectation, with 74% leaf-bending. The cultivars with a Deli × La Mé and Coarí × La Mé genetic background were the most tolerant; however, the Deli × AVROS and Deli × Yangambi genetic crosses were the most susceptible. The difference in the affectation between the groups was 60% to 70%. Leaf-bending affected physiological parameters such as photosynthesis, transpiration, and stomatal conductance. Thus, below the second ring of leaves, the affected plants’ physiological parameters decreased between 40% and 50%. The nutritional diagnosis showed that the most sensitive cultivars to leaf-bending were Deli × AVROS, which presented the highest average index of nutritional balance (IBNm), indicating that this genetic cross had the highest nutritional imbalance. On the contrary, the most tolerant cultivars were Deli × La Mé, which presented the lowest IBNm, associated with a better nutritional condition.

1. Introduction

Oil palm (Elaeis guineensis Jacq.) is the top oil-producing crop worldwide, making up over 36% of all oil production. Indonesia and Malaysia produce 84% of the world’s palm oil. Colombia is the fourth-largest palm oil producer globally, after Indonesia, Malaysia, and Thailand, leading Latin America in palm oil production. There are 595,722 hectares of oil palm plantations in Colombia [1]. These plantations mainly consist of two types: the tenera type palm (dura × pisifera) of the E. guineensis species, also known as African palm, and the interspecific OxG hybrids (E. oleifera × E. guineensis), a cross between American and African oil palms, which are resistant to diseases like bud rot [2,3].

Different physiological processes are studied in plants under abiotic stresses, such as water relations, nutrition, photosynthesis, and chlorophyll a fluorescence. Interestingly, the leaf area is one key trait determinant of the physiological capacity of plants to withstand some of the stress conditions. Furthermore, the leaf area is directly related to plant growth and development, dry matter accumulation, yield, and, in general, to the productive performance of crops [4,5]. The amount of light a plant intercepts depends strongly on the leaf area and other traits such as plant architecture, leaf length, individual leaf area, and leaf angles [6]. All these parameters are relevant to light distribution within the plant and, consequently, greatly influence self-shading, photosynthesis, and productivity [7,8].

The oil palm has indeterminate growth and can reach up to 30 m in height. In commercial plantations, it is advisable to renew the crop at 25 years of age, which can exceed 12 m in height [9]. In its mature stage, it has a crown that reaches between 40 and 50 open leaves. The leaves are 5 to 9 m long and are present in different stages of development, arranged on a pseudostem or on a single cylindrical stem [5]. Under favorable climatic conditions, the apical meristem can produce a new leaf primordium every two weeks in mature palms and every nine days in the juvenile stage [10,11]. The number of leaves produced at eight years of age can be between 20 and 25. These leaves are active for about 21 months [12].

Various limiting factors associated with oil palm cultivation can reduce the leaf area and yields. Those factors can be biotic [13,14,15] and abiotic factors [16,17,18] or genetic or physiological disorders. There is a disorder that significantly affects the oil palm canopy; this disorder, commonly known as leaf-bending, is characterized by a bending or arching of the leaves, which represents a twisting or breaking of the rachis of mature leaves with the formation of an angle greater than 180º in the vertical of the stem of the plant. The leaf-bending in the most advanced stages results in the petiole breaking and represents a significant challenge for oil palm cultivation. The leaf-bending reduces the number of effective leaves (leaves that are photosynthetically active and export photoassimilates to other parts of the plant). It could accelerate senescence, reducing fresh fruit bunch (FFB) production [19].

The leaf-bending manifests after severe drought and can persist a year after the dry periods. However, leaf-bending can also occur during the rainy season and in irrigated plantations, which rules out a direct relationship between leaf-bending and water deficit. Furthermore, soil properties such as texture, bulk density, infiltration, gravimetric moisture content, and moisture retention do not directly cause leaf-bending [19].

Although leaf-bending in oil palm plantations is known, its effect on palm performance and possible causes are unknown. For this reason, this work aimed to develop a quantitative methodology to estimate the degree of leaf-bending present in different oil palm cultivars and its effect on the plants’ physiology. In addition, the relationship between leaf-bending and the nutritional status of plants should be established through the nutritional balance index.

2. Materials and Methods

2.1. Location

The research was carried out in the Palmar de La Vizcaína Experimental Field of the Colombian Oil Palm Research Center (CENIPALMA), municipality of Barrancabermeja, Santander (Colombia), located at 6°59″03.2″ N and 73°42″21.1″ W, at an altitude of 102 m.a.s.l., with an average temperature of 29.3 °C, relative humidity between 72% and 77%, sunshine of 2020 h per year, and average annual rainfall of 3472 mm. The experiment’s soils were characterized by a clay and silty clay texture, a pH between 4.7 and 5.1, and 2.10% organic matter.

2.2. Plant Material

The genotypes evaluated correspond to Elaeis guineensis tenera type palm (dura × pisifera) and the interspecific OxG hybrid cultivars (E. oleifera × E. guineensis). The African oil palm cultivars came from three contrasting crosses in which the common female parent was Deli dura with three different male origins: AVROS, Nigeria, and La Mé (

Table 1. Commercial cultivars tenera (dura × pisifera) and interspecific O×G hybrids (E. oleifera × E. guineensis) used in the leaf-bending incidence study under the conditions of the Palmar de la Vizcaína Experimental Field (CEPV), Barrancabermeja, Colombia.

Cultivar	Name	Genetic Crossbreeding	Type
C1	AAR	Deli × AVROS Dumpy	tenera
C2	CORPOICA	Deli × (La Mé, Pobe) Yangambi)	tenera
C3	DAMI 103,101	Deli × AVROS	tenera
C4	DAMI 104,404	Deli × AVROS	tenera
C5	DAMI 114,112	Deli × AVROS	tenera
C6	ASD DXG	Deli × Ghana	tenera
C7	ASD DXN	Deli × Nigeria	tenera
C8	FELDA	Deli × Yangambi	tenera
C9	GOLDEN	Deli × AVROS	tenera
C10	GUTHRIE	Deli × Yangambi	tenera
C11	IOI	Deli × AVROS Dumpy	tenera
C12	IRHO 1001	Deli × La Mé	tenera
C13	IRHO 1401	Deli × La Mé	tenera
C14	IRHO 2528	Deli × La Mé	tenera
C15	OxG 2777	Coari × La Mé	O×G Hybrid
C16	OxG 2783	Coari × La Mé	O×G Hybrid
C17	UNIPALM Y22683	(Dejongo × Ekona) × Yangambi	tenera
C18	UNITED	Deli × (AVROS × Yangambi)	tenera
C19	UNIPALM Y22931	(Djongo × Ekona) × Yangambi	tenera
C20	OxG 2803	Coari × La Mé	O×G Hybrid
C21	EKONA COMPACT	Compact × Ekona	tenera
C22	COMPACTA GHANA	Compact × Ghana	tenera

). The interspecific OxG hybrids were Coari × La Mé. At the time of the first leaf-bending evaluation, the plants had been planted for 14 years in the field at 9 m between palms and a density of 143 plants per hectare.

2.3. Experimental Design

A randomized complete block design (RCBD) with 22 treatments and four replications was used. The treatments consisted of the oil palm genotypes described in Table 1 and established in June 2003. The experimental unit consisted of 20 plants, for a total of 80 palms per cultivar.

The evaluated cultivars originate from seeds imported from Malaysia, supplied by six producers from this country: Applied Agricultural Research (AAR), Golden Hope Plantations (GH), Guthrie Plantations, IOI Corporation, Federal Land Development Authority (FELDA), and United Plantations (UP). The local commercial cultivars were selected based on the frequency and area planted in oil palm regions in Colombia, as well as the relevance of the genetic nature of the progenitors [20,21].

2.4. Leaf Variables Measured

Figure 1 describes the position of the leaf in the phyllotaxis and the number of leaves according to the foliage (ring) level in the palm canopy [5]. Leaf-bending was evaluated in the different oil palm cultivars by counting the number of affected palm leaves in each leaf ring. The leaf-bending evaluation was performed every year for four consecutive years.

The following variables were measured:

(1)

Percentage of leaf-bending in the plant phyllotaxy: ratio between the number of affected leaves and the total number of leaves present in each ring. Corresponds to the severity of the disorder in each leaf ring.

(2)

Percentage of leaf-bending for each cultivar: ratio between the number of healthy plants (absence of affected leaves) and the number of affected plants (with at least one affected leaf) in each cultivar. Corresponds to the leaf-bending incidence.

(3)

Number of affected leaves per plant: ratio between the total number of affected leaves and the total number of leaves per plant. Corresponds to the leaf-bending severity.

2.5. Physiological Parameters

Under standardized conditions, gas exchange measurements were conducted using a portable gas exchange analyzer (LI-6800, Li-Cor, Lincoln, NE, USA) [22] in three contrasting cultivars, one susceptible, one resistant, and one intermediate, chosen from the 22 original cultivars, according to the incidence and severity measured before. The parameters in the measurement chamber were set as follows: CO₂ concentration at 400 ppm, relative humidity at 65%, airflow at 170 µmol s⁻¹, and photosynthetically active radiation at 1000 µmol m⁻² s⁻¹. The measured variables included assimilation (photosynthesis rate, µmol CO₂ m⁻² s⁻¹), stomatal conductance (mol H₂O m⁻² s⁻¹), and transpiration (mmol H₂O m⁻² s⁻¹). Measurements were taken between 8:30 and 11:30 a.m. on one leaf from each leaf ring. Specifically, leaves numbered 5, 13, 21, 29, and 37 were evaluated. For each leaf, three leaflets from the upper part of the lamina (sun leaflets) located in the central zone of the leaf were assessed.

2.6. Nutritional Balance

The nutritional diagnosis of the two most contrasting cultivars and an intermediate cultivar in leaf-bending incidence was carried out to evaluate the role of nutrition in the disorder. The DRIS (Diagnosis and Nutritional Recommendation Integrated System) indices [20,23] were obtained from historical records of leaf contents in contrasting cultivars according to the susceptibility to leaf-bending. The diagnosis was made by calculating indices (DRIS indices) from the average of functions estimated from the bivariate relationships between each nutrient considered in the analysis and the other elements, according to the methodology described [20], and adjusted for oil palm [21,24,25]. The DRIS indices are negative or positive depending on whether the element is deficient or excessive. Thus, the DRIS allows for the establishment of the order of requirements to be considered in nutritional management.

To evaluate the degree of nutrient sufficiency, the interpretation of the DRIS indices was complemented with the calculation of the average nutritional balance index (IBNm) from the sum of the absolute values of the DRIS indices of all the elements of the analysis. A crop in optimal nutritional balance presents IBNm values close to zero. Conversely, as IBNm increases, so does the degree of nutritional imbalance.

2.7. Statistical Analysis

For each response variable, analysis of variance, Tukey’s comparison tests, and mean contrasts using Scheffe’s test were performed. The R Studio software version 4.1.3 was used for all statistical analyses, using the packages ggplot2, Agricolae, and Performance.

3. Results

3.1. Disorder Description

The disorder known as leaf-bending in the oil palm crop can occur in any of the plant’s five levels of the leaf rings according to the phyllotaxis. The most characteristic symptom is the breaking of the petiole (Figure 2A,B), which begins with slight tears that increase in depth, causing openings or severe cracks in the petiole, ultimately bending the leaf completely (Figure 2C,D).

There were highly significant differences among the cultivars evaluated in all the years (p ≤ 0.001) (

Table 2. Analysis of variance (ANOVA) for incidence and severity of leaf-bending in oil palm cultivars across each evaluation period.

Response Variable *	Statistics	Year 1	Year 2	Year 3	Year 4
Affected palms per cultivar (%)	GL	21	21	21	21
	F value	19.03	16.36	38.83	23.58
	P(>F)	***	***	***	***
Leaves affected per palm per cultivar	GL	21	21	21	21
	F value	11.22	13.08	20.48	16.9
	P(>F)	***	***	***	***

* “Affected palms per cultivar” corresponds to incidence and “Leaves affected per palm per cultivar” corresponds to severity; GL: degrees of freedom; F value: value significant; P(>F): *** p > 0.05 significant.

). The most severe leaf-bending was observed in leaf rings three and four, where leaves 18 to 33 are located according to the phyllotaxis, with an average of 74% affectation, followed by 20% affectation in leaf ring five, corresponding to leaves 34 to 41. Finally, 6% leaf-bending in leaf rings one and two, corresponding to leaves 1 to 17 (Figure 3).

3.2. Leaf-Bending Affectation Per Cultivar

The incidence of leaf-bending in the first year of the evaluation showed that the cultivar DAMI-103-101 (Deli × AVROS) was the most affected by the disorder, with 70% of the plants showing leaf-bending, followed by the cultivars AAR and GUTHRIE with 55% each. Deli × La Mé IRHO-1001, IRHO 1401, and all OxG hybrids with palm affectation below 1% were the least affected cultivars. In the second year of evaluation, the leaf-bending incidence in the DAMI-103-101 cultivar continued to be the highest, with 77% of the plants affected, followed by GUTHRIE with 62%; however, the least affected cultivars for this year were the IRHO (1001 and 1401) and O×G hybrids, with percentages of palms affected below 2%.

The leaf-bending was most severe in the third year of the evaluation, with 93% to 97% of the Deli × AVROS plants affected. The least affected cultivars continued to be the O×G hybrids, with 1% to 5% of the plants showing symptoms of the disorder. In the last year of evaluation, the most affected cultivars were the Deli × AVROS, with 80% to 92% of palms affected, and the least were the O×G hybrids and the IRHO cultivars, with 3% of the palms affected.

In general, the trend was similar among the years evaluated, with the cultivars with the Deli × AVROS and Deli × Yangambi genetic backgrounds being the most affected and the Deli × La Mé and Coari × La Mé genetic crosses being the least affected (Figure 4).

3.3. Number of Affected Leaves Per Plant

The severity of the disorder showed highly significant differences among the evaluated cultivars in all the years (p ≤ 0.001, Table 2). In the first year of evaluation, the cultivar DAMI-103-101 had the highest number of affected leaves, with 4.1 leaves affected per plant. During the second and third years of evaluation, the Deli × AVROS and Deli × Yangambi cultivars presented the lowest number of affected leaves. Conversely, the Deli × La Mé and Coari × La Mé cultivars had the least affected leaves.

Finally, in the fourth year of evaluation, the cultivars most affected by the disturbance were DAMI-103-101, with 6.6 leaves affected per plant. The cultivars with the lowest affectation were IRHO-1401, O×G-2803, IRHO-1001, and O×G-2783, which had no affected leaves or, in some genotypes, very few leaves with a severity of less than 0.1 leaves per plant. In general, two contrasting groups of tolerant and resistant genotypes were formed. One group comprises the susceptible cultivars Deli × AVROS and Deli × Yangambi. The other group comprised the resistant cultivars formed by the Deli × La Mé and Coari × La Mé genetic crosses (Figure 4).

The contrasts of means analyzed with Scheffé’s test further confirmed the groupings of resistant and susceptible cultivars based on the disorder’s incidence (

Table 3. Comparative analysis of leaf-bending percentage in commercial tenera (dura × pisifera) and interspecific O×G hybrids (E. oleifera × E. guineensis) using contrasts.

Contrast	Difference in (%) of Bending	Pr > F	Significance	LL (α = 95%)	UL (α = 95%)
Deli × La Mé vs. all others	−38.00	0.000	***	−54.91	−21.10
Coari × La Mé vs. all others	−40.71	0.000	***	−60.83	−20.59
Deli × AVROS vs. all others	39.04	0.000	***	22.13	55.94
Deli × La Mé vs. Deli × AVROS	−65.49	0.000	***	−87.53	−43.45
Coari × La Mé vs. Deli × AVROS	−69.82	0.000	***	−94.46	−45.18
Deli × La Mé vs. Deli × Yangambi	−55.68	0.000	***	−80.32	−31.04
Coari × La Mé vs. Deli × Yangambi	−60.01	0.000	***	−87.01	−33.02
Deli × AVROS vs. Deli × Yangambi	9.80	0.998	ns	−14.83	34.44
Deli × La Mé vs. Deli × Ghana	−43.61	0.000	***	−74.78	−12.44
Deli × La Mé vs. Deli × Nigeria	−30.19	0.072	ns	−61.36	0.96
Deli × AVROS vs. Deli × Ghana	21.87	0.635	ns	−9.29	53.04
Deli × AVROS vs. Deli × Nigeria	35.29	0.008	**	4.12	66.46

*** Highly significant differences p ≤ 0.001. ** Highly significant differences p ≤ 0.01. ns = No significant differences. LL = Lower limit of the 95% confidence interval for the difference in bending percentage. UL = Upper limit of the 95% confidence interval for the difference in bending percentage.

) and severity (

Table 4. Comparative analysis of the number of affected leaves per plant in commercial tenera (dura x pisifera) and interspecific O×G hybrids (E. oleifera × E. guineensis) using contrasts.

Contrast	Difference in Number of Sheets	Pr > F	Significance	LL (α = 95%)	UL (α = 95%)
Deli × La Mé vs. other cultivars	−2.49	0.00006	***	−4.22	−0.76
Coari × La Me vs. other cultivars	−2.42	0.00441	**	−4.47	−0.36
Deli × AVROS vs. other cultivars	2.66	0.00001	***	0.94	4.39
Deli × La Mé vs. Deli × AVROS	−4.38	0.00000	***	−6.63	−2.13
Coari × La Mé vs. Deli × AVROS	−4.44	0.00000	***	−6.96	−1.93
Deli × La Mé vs. Deli × Yangambi	−4.84	0.00000	***	−7.35	−2.32
Coari × La Me vs. Deli × Yangambi	−4.91	0.00000	***	−7.65	−2.14
Deli × AVROS vs. Deli × Yangambi	−0.45	1.00000	ns	−2.97	2.06
Deli × La Mé vs. Deli × Ghana	−1.99	0.82710	ns	−5.17	1.18
Deli × La Mé vs. Deli × Nigeria	−1.06	0.99993	ns	−4.24	2.12
Deli × AVROS vs. Deli × Ghana	2.39	0.48731	ns	−0.78	5.57
Deli × AVROS vs. Deli × Nigeria	3.32	0.02826	*	0.14	6.51

*** Highly significant differences p ≤ 0.001. ** Highly significant differences p ≤ 0.01. * Significant differences p ≤ 0.05. ns = No significant differences. LL = Lower limit of the 95% confidence interval for the difference in the number of bent leaves. UL = Upper limit of the 95% confidence interval for the difference in the number of bent leaves.

). In terms of incidence (number of palms affected per cultivar), the comparison of the least affected E. guineensis cultivar, Deli × La Mé, with the other cultivars showed a high significance (p ≤ 0.001) and a 38% reduction in the percentage of affected leaves in this cultivar; a similar behavior was observed when comparing the interspecific O×G hybrids, Coari × La Mé, with the other cultivars (high significance p ≤ 0.001), where O×G had 40% less leaf-bending. On the other hand, the comparison between the Deli × AVROS genetic background and the other crosses showed highly significant differences (p ≤ 0.001), with 39% more leaf-bending compared to the other cultivars evaluated (Table 3).

When comparing the two tolerant cultivars Deli × La Mé and Coari × La Mé with the most susceptible cross Deli × AVROS, they showed high significance (p ≤ 0.001) with values of 65% and 69% less damage in the resistant cultivars, compared with the susceptible. Likewise, the cultivars with the Deli × Yangambi genetic background, also susceptible to the disorder, showed similar behavior to the Deli × AVROS cultivar when compared to the tolerant cultivars (Deli × La Mé and Coari × La Mé), finding significant differences (p ≤ 0.001) with values of 55% and 60% more, respectively. In this sense, no significant differences were found when comparing the two cultivars with higher susceptibility, Deli × AVROS vs. Deli × Yangambi (Table 3).

Regarding severity, which corresponds to the number of leaves affected per plant, the comparison between the Deli × La Mé cultivar and the other cultivars showed high significance (p ≤ 0.001), with less than 2.49 leaves affected per plant. A similar behavior was presented when comparing the interspecific hybrid Coari × La Mé with the other cultivars (high significance p ≤ 0.001), where the difference was less than 2.42 leaves affected per plant. The comparison between the most susceptible cultivar (Deli × AVROS) and the other cultivars showed highly significant differences (p ≤ 0.001), with 2.66 more leaves affected. In addition, comparisons of the two most tolerant crosses (Deli × La Mé and Coari × La Mé) with the most susceptible Deli × AVROS showed high significance (p ≤ 0.001) with 4.38 and 4.44 fewer leaves affected, respectively. Similarly, when comparing Deli × Yangambi with the most tolerant cultivars, highly significant differences were found (p ≤ 0.001), with 4.8 more leaves affected. No significant differences were found when comparing Deli × AVROS with Deli × Yangambi (Table 4).

3.4. Effect of Leaf-Bending on the Gas Exchange Parameters

Under adequate growth conditions, the photosynthetic rate, transpiration, and stomatal conductance of palm leaves are highest in the middle leaves of rings one and two. In the first leaf ring, photosynthesis was higher, with an average of 14.6 µmol CO₂ m⁻² s⁻¹, and decreased progressively with leaf age, reaching an average of 6.3 µmol CO₂ m⁻² s⁻¹ in the fifth leaf ring. Transpiration in healthy leaves was also higher, averaging 5.3 mmol H₂O m⁻² s⁻¹ in leaves of levels one and two, and decreasing progressively to between 3.1 and 4.6 mmol H₂O m⁻² s⁻¹ in rings three and four, respectively, and 2.6 mmol H₂O m⁻² s⁻¹ in ring five. Similarly, stomatal conductance showed a similar trend, with values of 0.40 and 0.38 mol H₂O m⁻² s⁻¹ in leaves evaluated in rings one and two, respectively, decreasing progressively to 0.17 mol H₂O m⁻² s⁻¹ in ring five. On the other hand, the leaves with leaf-bending symptoms showed reductions in photosynthesis, stomatal conductance, and transpiration. Although there were no leaves with defoliation in ring one, this effect was present from ring two onward, with progressive reductions of more than 40% in all physiological variables up to ring five.

Gas exchange behavior was studied in three contrasting cultivars, which had been previously classified as tolerant (Deli × La Mé, C12), intermediate (Deli × Nigeria, C7), and susceptible (Deli × AVROS, C3) according to their leaf-bending incidence and severity. The palms of Deli × La Mé did not have bent leaves in any of their leaf rings. In leaf rings one, two, and three, photosynthetic rates between 12 and 15 µmol CO₂ m⁻² s⁻¹, transpiration between 5 and 6.1 mmol H₂O m⁻² s⁻¹, and stomatal conductance between 0.34 and 0.43 mol H₂O m⁻² s⁻¹ were measured. Deli × Nigeria showed bent leaves in leaf rings three, four, and five. Healthy non-bent leaves had photosynthetic rates similar to those of Deli × La Mé, with a progressive decrease with leaf age. However, the gas exchange parameters in leaves with some degree of leaf-bending suffered a decline between 40% and 53% in photosynthesis, 49% and 66% in transpiration, and 54% and 71% in stomatal conductance.

The susceptible Deli × AVROS cultivar showed a more significant number of leaves and rings affected by defoliation. In rings two and three, there were reductions in photosynthesis of 45% and 57%, transpiration of 38% and 67%, and stomatal conductance of 40% and 71%. In leaf ring five, there were no healthy leaves, and all the leaves evaluated showed severe bending at the level of the petiole, which led to a general drying of the leaflets and, therefore, very low values for the variables evaluated (Figure 5).

3.5. Nutritional Status and Leaf-Bending

Table 5. Multiannual mean values of foliar nutrient contents in three E. guineensis oil palm cultivars with varying resistance levels to leaf-bending.

Cultivar	N	P	K	Ca	Mg	Cl	S	B	Faith	Cu	Mn	Zn
	%							mg kg−1
Sufficiency range	2.20–2.47	0.14–0.17	0.74–0.92	0.63–0.73	0.19–0.26	0.56–0.71	0.15–0.17	20–23	60–67	5.9–6.9	686–833	22–26
Deli × AVROS	2.22	0.14	0.69	0.63	0.32	0.60	0.18	21.78	75.91	6.44	984.69	26.93
Deli × Nigeria	2.31	0.14	0.90	0.57	0.22	0.63	0.18	22.68	78.48	5.97	846.86	22.67
Deli × La Mé	2.33	0.14	0.83	0.52	0.22	0.60	0.19	26.20	61.94	5.58	866.73	17.19

shows the multiannual nutrient contents of the most leaf-bending susceptible cultivar (Deli × AVROS), the most resistant cultivar (Deli × La Mé), and a cultivar with intermediate resistance to the disorder (Deli × Nigeria). Based on these data, the nutritional status of the plants was interpreted using the Diagnosis and Recommendation Integrated System (DRIS), and nutrients were classified in terms of deficiency, sufficiency, or excess, considering the parameters described in

Table 6. Interpretation of the DRIS indices.

Criteria	Nutritional Status
DRIS < 0 and |DRIS| > IBNm	Deficient
|DRIS| ≤ IBNm	Balancing
DRIS > 0 and |DRIS| > IBNm	Excess

.

Table 7. Nutrient balance of three E. guineensis oil palm cultivars with varying resistance levels to leaf-bending according to the DRIS method.

Crossover	DRIS indices												IBNm
	N	P	K	Ca	Mg	Cl	S	B	Faith	Cu	Mn	Zn
Deli × AVROS	−5.6	−15.5	−10.6	−8.2	10.5	−5.6	7.1	3.2	12.4	−3.2	11.4	4.1	6.7
Deli × Nigeria	−1.7	−12.3	2.3	−12.7	−1.4	−1	8.2	4.1	21.4	−6.9	5	−4.9	6.2
Deli × La Mé	4.9	−5.8	2.6	−15.5	0.6	0.3	15.8	18	2.6	−10.8	8.2	−20.7	4.7

shows the calculated DRIS indices per nutrient for the three cultivars evaluated and the IBNm. In the three cultivars, the calculated DRIS indices showed negative phosphorus, calcium, and copper values, while positive values were found for sulfur, boron, iron, and manganese.

In addition to the abovementioned elements, the Deli × AVROS (susceptible) cultivar had negative DRIS indices for nitrogen, potassium, and chlorine, while zinc had positive values. This behavior was opposite to that of the tolerant Deli × La Mé.

On the other hand, the results showed that IBNm increased with the degree of palm susceptibility to leaf-bending. Thus, the most susceptible cultivar, Deli × AVROS, presented the highest IBNm, indicating that this cultivar had the highest nutritional imbalance. On the contrary, the tolerant cultivar Deli × La Mé had the lowest IBNm, indicating a better nutritional status. The intermediate cultivar Deli x Nigeria presented a similar nutritional balance to the cultivar Deli × AVROS.

Table 8. Classification of nutrients by degree of sufficiency and order of requirement in three E. guineensis oil palm cultivars with varying resistance levels to leaf-bending.

Crossover	Order of Injunction
	Deficient	Enough	Excess
Deli × AVROS	P > K > Ca	N > Cl > Cu > B > B > Zn	S > Mg > Mn > Fe
Deli × Nigeria	Ca > P > Cu > Zn	N > Mg > Cl > K > K > B	Mn > S > Fe
Deli × La Mé	Zn > Ca > Cu	P > Cl > Mg > Fe > K > K > N	Mn > S > B

classifies nutrients according to their degree of sufficiency and order of requirement. This classification indicates that calcium is deficient in all three cultivars, while phosphorus is limited in the most susceptible cultivars.

4. Discussion

The optimal number of functional green leaves in oil palm is between 32 and 40 [5]. Any biotic or abiotic factor that limits an adequate leaf area is detrimental to the proper functioning of the palm and has a negative impact on fruit bunches and oil production [19]. The leaf-bending syndrome significantly affects the functional leaf canopy of the palm, as evidenced by the number of affected leaves found in the most susceptible cultivars, with the common male genitors AVROS and Yangambi and the phyllotaxy position of these affected leaves, which reduced production, nutritional, and vegetative parameters in the affected leaves.

Leaf-bending exhibited a consistent behavior across the four years of evaluation, forming two distinct groups of cultivars based on their response. One group included the genetic crosses Deli × AVROS and Deli × Yangambi, which were the most susceptible. The other group consisted of Deli × La Mé and Coari × La Mé, which were the most tolerant. The Deli × La Mé cross and the OxG interspecific hybrids Coari × La Mé showed higher tolerance to leaf-bending, with almost no leaves affected. Conversely, the Deli × AVROS cross was the most susceptible, with leaves affected starting from leaf ring two and very severe bending in the fifth leaf ring, accompanied by senescence and drying of leaflets. Interestingly, the O×G hybrids showed the lowest affectation, or in some cases, no leaf-bending, indicating strong resistance to this disorder.

The physiological impact of leaf bending is profound. Gas exchange parameters, including net photosynthesis, transpiration, and stomatal conductance, were significantly reduced in affected leaves. In a healthy palm, photosynthesis in the upper leaf rings is high, and it is natural for this value to decrease as the leaves age [18]. Our study presented values above 13 µmol CO₂ m⁻² s⁻¹, similar to those reported by Bayona-Rodríguez and Romero [26], and as the leaves aged, net photosynthesis was reduced to 6.3 µmol CO₂ m⁻² s⁻¹ in the fifth leaf ring in unaffected leaves. However, in plants with leaf bending, photosynthesis was reduced by almost 50% in the affected upper rings, reaching values close to zero in the lower canopy rings in severe cases.

This reduction in photosynthetic capacity is likely due to the breakage or bending of the petiole bases of the leaves, which limits the water supply to the leaflets, causing stomatal closure and reduced CO₂ assimilation. Under water stress, a decrease in vegetative growth, leaf water content, stomatal conductance, transpiration rate, and net photosynthesis have been found [27]. Additionally, the curvature of the petiole bases can result in self-shading within the palm canopy or changes in leaf exposure angles, reducing light interception [28,29]. Furthermore, severe damage to the petiole bases leads to wilting and senescence of the leaves, reducing the number of photosynthetically active leaves and impacting fresh fruit bunch (FFB) production [30].

The impact of leaf-bending on oil palm productivity is multifaceted. The disruption in photosynthetic efficiency, combined with the structural damage to the leaves, significantly reduces the plant’s overall energy production. Research studies on different oil palm genotypes have reported significant differences in gas exchange, photochemical activity, and other biochemical responses [31,32,33,34]. This reduction affects the current year’s yield and can have long-term effects on the palm’s health and productivity [31]. Over time, the cumulative impact of reduced photosynthesis and increased leaf senescence can lead to a decline in fruit production and overall palm vitality [35].

Nutritional diagnosis revealed the highest nutrient imbalance in the susceptible Deli × AVROS and Deli × Yangambi genetic crosses, indicated by high IBNm values. Conversely, the resistant Deli × La Mé and Coari × La Mé crosses had the lowest IBNm, indicating better nutritional status. The DRIS system diagnosed nutrient deficiencies, showing calcium was deficient in all the cultivars, while phosphorus was limiting in the most susceptible cultivars. Potassium deficiency in the most susceptible cultivar (Deli × AVROS) also likely contributed to leaf-bending, as potassium is crucial for maintaining plasma membrane turgor and stomatal function [36]. This deficiency has been previously linked to leaf-bending disorder [19].

Leaf-bending due to water deficit has been reported in oil palm areas of Costa Rica. Bent leaves remain with their stomata closed during the day, affecting their photosynthetic capacity and nutrient translocation [37]. Susceptible cultivars may keep their stomata open longer than tolerant ones, exacerbating water loss and nutrient imbalances [26].

The findings of this study highlight the importance of selecting and breeding oil palm cultivars with inherent resistance to leaf-bending. Cultivars with a genetic background of Deli × La Mé and Coari × La Mé have shown promising tolerance, suggesting that these genetic lines should be prioritized in breeding programs and present a viable strategy for improving oil palm productivity in regions prone to these disorders.

From a management perspective, regularly monitoring the nutritional status of oil palms is crucial. Ensuring that palms receive adequate and balanced nutrition can mitigate the effects of leaf-bending. The use of the DRIS system provides a reliable method for diagnosing and addressing nutrient deficiencies, helping to maintain the health and productivity of the palms. Put this way, better agricultural practices and adopting technologies, including balanced nutrition, will enhance the production of fresh fruit bunches per hectare in various oil palm plantations [19].

5. Conclusions

The methodology developed in this study provides a robust framework for quantifying leaf-bending in oil palm cultivars. This quantitative approach allows for the accurate assessment of cultivar susceptibility and provides a basis for informed decision-making in breeding and management practices.

For this case study, the genetic crosses that include AVROS male parents presented an average of 10 affected leaves compared to La Mé male parents. On the other hand, in the physiological parameters evaluated, the most susceptible cultivars showed reductions between 40% and 71%. The mean nutritional balance index (IBNm) increased with the degree of susceptibility of the palms with the most affected leaves in those crosses with AVROS male parents.

Focusing on resistant cultivars and maintaining optimal nutritional balance can mitigate the impact of leaf-bending and enhance the productivity and sustainability of oil palm plantations.

Future research should continue to explore the genetic and environmental factors contributing to leaf-bending, emphasizing identifying the underlying resistance mechanisms. Additionally, long-term studies on the impact of leaf-bending on oil palm productivity and health will provide valuable insights into managing this disorder. Implementing these strategies will help ensure the continued success of oil palm cultivation in the face of biotic and abiotic challenges.