1. Introduction

Cashew (Anacardium occidentale L., Anacardiaceae) is a tree species that is native to Brazil [1]. Cashew was first introduced to Côte d’Ivoire in 1951 to reforest cutover lands, and mitigate soil erosion [2]. Between 1959 and 1960, cashew forest plantation programs were implemented by seeding nuts in the northern and central parts of Côte d’Ivoire and, subsequently, throughout the entire Sudano-Guinean savanna zone [2]. Since 2015, Côte d’Ivoire has become the world’s largest producer of cashew nuts, producing 700,000 tons in 2015 [3]. Production exceeded more than one million tons in 2022 [4]. MINADER showed approximately 330,000 households (about 1.9 million people) would be involved in cashew production, making it the most important source of income in rural areas in the northern part of the country [5]. This crop contributes to the acquisition of goods and services by producers in Côte d’Ivoire. For instance, [6] showed that at the end of each season, cashew marketing improved annual net income per hectare by 78–80% of the average annual income received by households in Côte d’Ivoire.

However, the low diffusion of improved planting materiel, the strong pressure from pests and a lack of adoption, combined these issues result in   relatively low nut yields (524 kg ha^-1 on average) compared to the minimum of 1,000 kg ha^-1 harvested from orchards in India and Brazil. Thus, it is important to delineate the phenological growth stages of the cashew trees in Côte d'Ivoire. For instance, [7] stated that mastering the phenology of crop species improves the effectiveness and efficiency of crop management practices, varietal improvement programs, and germplasm characterization.

The proper understanding of cashew phenological growth stages may contribute to more efficient planning of management practices of this important crop, to optimize production in Côte d'Ivoire. In this context, this   study aimed to describe the complete floral and fruit development stages in cashew according to the BBCH scale.

2.  Materials and methods

2.1  Plant material

Plant material included 21 grafted cashew genotypes. These genotypes were selected based on the nut yield of their mother trees and on the basis of their high kernel content (Table 1). The study area coincided with the sub- prefecture of Badikaha (Hambol region), which is located in the north- central region of Côte d'Ivoire. The experimental site was located 6 km from the town (9° 12' north; 5° 10' west; Fig. 1). The climate of this region is tropical, and is characterized by two alternating seasons: a rainy season from May to September, and a dry season from October to April. The average annual temperature is 25.9 °C. The average annual rainfall is 1130 mm, in 2021. The soil of the region is ferralitic type, which is predominantly clayey- sandy and gravelly [19]. The vegetation is dominated by clear forest (wooded savanna) and wooded savanna [16].

Table 1. Origin and characteristics of the mother trees of the 21 cashew genotypes used in the present study

Regions / Localities	Genotypes	Origin	Yields (kg/tree)		Percentage Kernel Out-turn (%)		Age of trees in 2016 (year)
			2015	2016	2015	2016
Hambol / Badikaha (Tafiré) pour Katiola	KADM-98	Karakoro	34	39	27	22.9	16
	KADM-105		26.5	23	28.9	30.1	13
	KADM-181		20	9	32	25.5	16
	KADM-103		45	21.6	27.3	24.5	16
	KADM-96		-	15	25.8	25.0	16
	KADM-100		27	14.7	28.1	31.8	16
	KADM-84	Koni	48.5	32	42	26	25
	KADM-85		17.5	19	27.6	27.9	25
	KADM-112	Boundiali	10	39	28.6	27.2	18
	KADM-37		21.5	14	28.1	25.1	19
	KADM-106		-	11	29.2	29.2	18
	KADM-35		25.3	14.4	30	23.6	19
	KADM-87	Sinématiali	-	60.8	-	27.6	19
	KADM-90		-	28.7	-	27.1	19
	KADM-91		-	29	-	27	19
	KADM-76	Waraniéné	12.5	10.5	26.5	26.8	11
	KADM-195	Fronan	-	20	-	25.3	19
	KADM-189	Katiola	-	7,5	-	27.9	8
	LAX3264	Lataha	-	18a	-	27.09	31
	LAX4297		-	19 a	-	28.04	31
	LAZ330		-	13 a	-	28.53	31

a: Average yield (1994-2002) in kg of nuts/tree/year.

Figure 1. Location of the study area

2.2 Methods

A 1.5 ha orchard in Badikaha was established on September 15, 2016. The   site had a systematic, non-classical setup consisted of two blocks. The first block was complete with 21 genotypes. The second block was incomplete, and had 13 genotypes. The first block contained 336 plants (16 trees x 21). Each row had one genotype with 16 trees. A distance of 5 m was maintained between trees and genotypes. Five trees were observed (candidate trees) per genotype (Fig. 2).

Figure 2. Experimental device

Trees were selected based on the high number of shoots at stage 319 of the extended BBCH scale created by [8]. This stage represents the reference stage for the current study (Table 2). It is characterized by well-matured shoots  (fully developed dark green, leathery leaves). One-hundred and five trees were selected. Two twigs were then tagged in each cardinal direction on each candidate tree. Eight-hundred and forty twigs were labeled on the 105 selected trees. After tagging, twig evolution was monitored using the three-digit extended BBCH scale of [8]. Shoot development was observed daily from labeling to the end of flowering. After flowering, fruiting was observed every three days per week until ripening.

Table 2. Description of growth stage 3: shoot development.

Data were collected on the floral, fruiting, and yield traits of the 21 cashew genotypes. All data were collected over six months, from October 5, 2020, to April 5, 2021. The identified phenological growth stages were photographed with the digital camera (Nikon Coolpix W100).

3. Results and discussion

3.1  Variation in phenological stage

This study identified four major and 26 minor growth stages for cashews. The main flower growth stages were: two floral phenophase stages (inflorescence and flowering stage). These two main stages were formed of 15 secondary stages. Out of the 15 secondary stages of floral phenology, three secondary stages had not been previously recorded by [8]. These included two secondary stages within the main inflorescence stage (stages 510 and 513), and one secondary stage in the main flowering stage (stage 616). At the fruit level, two fruiting phenophase stages (fruit development and ripening stage), encompassing 11 secondary stages, were recorded. The secondary stage 714 that has been described in the current study was not observed by [8]. Thus, four secondary stages (510, 513, 616, and 714) of floral and fruiting phenophases were found in this current study.

Vegetative: For the 21 genotypes, bud break (i.e., end of vegetative growth stage and beginning of inflorescence stage) occurred at 6 weeks (from November 10, 2020) to 9 weeks (Table 3). It lasted 6 weeks in early flowering genotypes (KADM-103 and KADM- 195), 8 weeks in intermediate flowering KADM-100, KADM-35, LAX-3264, KADM-181, KADM-98, KADM-76, KADM-90, and KADM-96), and 9 weeks in late flowering genotypes (KADM-112, KADM-85, and LAX-4297).

Flowering: Intermediate and late flowering genotypes initiated reproductive buds (inflorescence stage) 2 weeks and 3 weeks after the early flowering genotypes, respectively (Table 3). For all three types of flowering genotypes, the transition from early flowering to 100% flowering spanned 5 weeks.

Fructification: The fruit development stage started 13, 15, and 16 weeks after bud break for early, intermediate, and late flowering genotypes (Table 3), respectively. For all three types, the transition from early fruiting to 100% fruiting spanned 3 weeks. There was a 7-week period between flowering and fruiting, regardless of genotype. Bud break to 100% fruiting required 16, 18, and 19 weeks for early, intermediate, and late flowering genotypes, respectively.

Table 3. Flowering and fruiting period of 21 cashew genotypes (S = weeks) 

	Flowering				Fructification
Genotype	Stage 319	Beginning	50٪	100٪	Beginning	50٪	100٪	Fl period
KADM-103	S0	S6	S9	S11	S13	S15	S16	Precocious
KADM-195	S0	S6	S9	S11	S13	S15	S16	Precocious
KADM-98	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-181	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-100	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-105	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-96	S0	S8	S11	S13	S15	S17	S18	intermediate
Lax-3264	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-84	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-106	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-37	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-35	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-87	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-90	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-91	S0	S8	S11	S13	S15	S17	S18	intermediate
Laz-330	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-76	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM-189	S0	S8	S11	S13	S15	S17	S18	intermediate
KADM -85	S0	S9	S12	S14	S16	S18	S19	belated
KADM-112	S0	S9	S12	S14	S16	S18	S19	belated
LAX-4297	S0	S9	S12	S14	S16	S18	S19	belated

 

Our study is in agreement with other studies using, in the last three decades, the extended Biologische Bundesantalt, Bundessortenamt and Chemische Industrie (BBCH) scale to describe the phenological stages [10] of several annual and perennial crops. Examples of crops include grapevine [12], citrus [13], guava [14], cocoa [11], mango [15], and cashew [8].

3.2  Flower development stages

Two stages of floral phenology were determined for cashew: the inflorescence stage and the flowering stage (Table 4). Inflorescence stage (stage 5): Eight secondary stages describing the inflorescence stage were delineated (Table 4). These are: 510; 511; 513; 514; 515; 516; 517 and 519. The inflorescence stage begins with secondary stage 510, which follows stage 319. Stage 510 is characterized by the initiation of the reproductive bud, marking the start of the swelling of the reproductive bud. Stage 513 then occurs at the start of panicle elongation. Stages 513, 514 and 515 are marked respectively by the development of floral buds passing through 3, 4 and 5 floral buds on the panicles during panicle development. Stages 516 and 517 represent the development of panicular branches.  Stage 519 marks the end of panicle development, with a network of swollen flower buds on the panicle branches.

Flowering stage (Stage 6): Seven secondary stages (Table 4) were recorded (610; 611; 613; 615; 616 and   617). The flowering stage begins with the opening of the first flower bud (stage 610), formed during the inflorescence stage, and ends at stage 619 (end of flowering and appearance of the first fruit set). The secondary stage 611 corresponds to 10% of flowers open (i.e. 10/100 flower buds open). The opening of 30% of flowers indicates secondary stage 613 (i.e. 30/100 flowers are open). Secondary stages 615 and 616, marked respectively by the opening of 50 and 60% (i.e. 50/100 and 60/100) of flowers. The 617 stage is characterized by the opening of 70% (i.e. 70/100) of the flowers and finally the 619 secondary stage with 90 to 100%  (i.e. 90/100 to 100/100) of the flowers open.

Table 4. Description of floral phenophases of 21 cashew genotypes

 3.3 Fruiting phenophases

Two stages of fruiting phenology were determined for cashews: the fruit development stage and the fruit ripening stage (Table 5). Fruit development stage (stage 7): This stage is composed of six sub-stages delimiting the development of the fruit (Table 5). These sub-stages are: 711, 713, 714, 715, 717 and 719. The fruit development stage begins with sub- stage 711, in which the nut is soft and represents about 10% of the final size (i.e. 10/100), and the apple represents about 2.5% of the final size (i.e. 2.5/100). The surface colour of the nut and apple was green. Stage 713 occurred later, with the nut at 30% of the final size (i.e. 30/100) and the apple at 5% of final size  (i.e. 5/100). The surface colour of the nut and apple was pink. Stage 714 Stages 715, 717 and 719 represent successive stages of development, with the nut reaching 40% of its final size. Stage 714 was missed in the study conducted by Adiga and colleagues [8]. This stage was highlighted in the present study, bringing to 11 the number of secondary stages of the fruiting phenophase described in the cashew tree. Stages 715, 717 and 719 represent successive stages of development, with the nut reaching 50%, 70% and 90% of its final size (i.e. 50/100, 70/100 and 90/100) and the apple reaching 7.5%, 10% and 15% of its final size (i.e. 7.5/100, 10/100 and 15/100). At these secondary stages (stages 715, 717 and 719), the nuts have become greener, with a visible ridge on the surface of the apple. Stage 719 represents the end of total cashew nut growth (physiological maturity of the nut), while the apple has continued to grow during the ripening phase.

Fruit ripening stage (stage 8): Five secondary stages of ripening was delineated (Table 5). These secondary stages are: 811, 813, 815, 817 and 819. The ripening stage begins at secondary stage 811, when the apple has reached about 20% of its final size (i.e. 20/100). The surface of the apple was light green, and the shell of the nut became dark green, with grey on its surface.

Table 5. Description of fruiting phenophases in 21 cashew genotypes.

At stage 813, the apple had reached around 30% of its final size (or 30/100). The surface of the apple remained light green, while the whole nut turned greenish grey and continued to harden. At stage 815, the apple has reached about 50% of its final size (50/100). The surface of the apple has taken on a yellowish colour and the nut has turned whitish grey. At stage 817, the apple has reached about 70% of its final size (70/100). The surface of the apple has begun to show shades of orange or red on the yellowish surface, while the nut has taken on an ashen colour. Stage 819  represents the end of the fruit's ripening phase. At this stage, the nut and apple were completely ripe (horticultural maturity of the fruit). The apple was at 90-100% (i.e. 90/100 or 100/100) of its final size.

3.4 Duration of secondary stages for floral and fruiting phenophases

In total, 26 flower and fruit phenophase substages were recorded in the 21 cashew genotypes (Table 6). The duration of the eight substages from the inflorescence stage was 74 days, on average. For the flowering stage, the seven secondary stages averaged 59 days. The six secondary stages of fruit development averaged 52 days. The fruit ripening stage lasted just 36 days, and had five secondary stages. The floral phenophases were the longest stages, with 15 secondary stages spanning 133 days, on average. Fruit phenology (with 11 secondary stages) lasted 88 days. Overall, the 26 secondary stages of the floral and fruiting phenophases lasted 221 days, on average. In the present study, the floral and fruiting phenophases lasted 133 and 88 days, respectively. These results supported those of [17], who showed that the anthesis of cashew flowers lasted about 150 days. Masawe et al. recorded inflorescences at different stages on the same tree, and even on the same inflorescence (flower buds, open flowers, fruit set, immature fruit, and mature fruit) [18]. This phenomenon is used to determine the type of maturity of cashew fruit (i.e., grouped, intermediate, or spread out). That could be one of the reasons that would explain the poor performance of cashew planting material used in Côte d'Ivoire. In the mango tree for example, the production cycle of the Cogshall variety of mango grown on St. Pierre (Reunion) lasts 1.5 years. This cycle is separated into four important periods (or phenological stages): vegetative growth, vegetative rest, flowering, and fruiting [9].

Table 6. Floral and fruiting phenophases secondary stages duration 

Main stage	Secondary stage	Duration of secondary stage
	Stages 319 to 510	8 days
	Stages 510 to 511	8 days
	Stages 511 to 513	11 days
	Stages 513 to 514	9 days
	Stages 514 to 515	8 days
	Stages 515 to 516	8 days
	Stages 516 to 517	8 days
	Stages 517 to 519	14 days
Stage of the inflorescence	Total duration	74 days, approximately 2.5 months
	Stages 519 to 610	4 days
	Stages 610 to 611	8 days
	Stages 611 to 613	8 days
	Stages 613 to 615	8 days
	Stages 615 to 616	10 days
	Stages 616 to 617	13 days
	Stages 617 to 619	8 days
Flowering stage	Total duration	59 days, approximately 2 months
	Stages 619 to 711	7 days
	Stages 711 to 713	9 days
	Stages 713 to 714	9 days
	Stages 714 to 715	9 days
	Stages 715 to 717	9 days
	Stages 717 to 719	9 days
Stage of fruit development	Total duration	59 days, approximately 2 months
	Stages 719 to 811	4 days
	Stages 811 to 813	9 days
	Stages 813 to 815	9 days
	Stages 815 to 817	7 days
Fruit ripening stage	Stages 817 to 819	7 days
	Total duration	36 days, approximately 1 month

 Total of days in the main stages: 221 days, about 7.5 months

 4.   Conclusions

This study identified four main growth stages and 26 secondary growth stages in 21 cashew genotypes grown in a wool field at Badikaha, Côte d’Ivoire, using the extended BBCH scale defined by. Of these 26 secondary stages, 15 and 11 were flower and fruit phenophases, respectively. The present study identified four previously undescribed secondary stages in cashew; three secondary stages, including two of inflorescence (secondary stages 510 and 513), and one of flowering (secondary stage 616). Another secondary stage of the fruiting phenophase was also identified (secondary stage 714). The description of the different phenological stages of the 21 cashew genotypes in this study provided tools for developing technical approaches to optimize production and creating new varieties through controlled hybridization.

Authors’ contributions

Conception, original idea, data collection, writing, analysis and statistical processing of data, C.K.K.; Drafting, correction and revision of the manuscript, F.L.; Research orientations and manuscript revision, A.K.J.; Guidelines, research orientations, drafting of the manuscript and review of previous versions of this article, C.K. K.

Acknowledgements

This study was financed by the Conseil du Coton et de l'Anacarde (Côte d'Ivoire) for the implementation of the National Cashew Research Programme (PNRA), coordinated by the Fonds Interprofessionnel pour la Recherche et le Conseil Agricoles (FIRCA).

Funding

This research received no external funding.

Availability of data and materials

All data will be made available on request according to the journal policy.

Conflicts of interest

The authors declare no conflict of interest.

References

1.         Trevian, M.T.S.; Pfundstein, B.; Haubner, R.; Würtele, G.; Spiegelhalder, B.; Bartsch,  H.; Owen, R.W. Characterisation of alkyl phenols in cashew (Anacardium   occidentale L.) products and assay of the antioxidant capacity. Food Chem. Toxicol.  2005, 44 (2), 188-197. https://doi.org/10.1016/j.fct.2005. 06.012.

2.         Goujon, P.; Lefebvre, A.; Leturcq, P.H.;  Marcellesi, A.P.; Praloran, J.C. Études sur l’anacardier. Bois Forets des Trop. 1973, 151, 27-53.

3.         Kouakou, C.K.; N’Da Adopo, A.A,; Djaha, A.J.B.; Minhibo, M.Y.; Djidji, A.H. Sélection de clones d’anacardier (Anacardium occidentale L.) de Côte d’Ivoire pour la qualité de la noix. In Proceedings Intensification agro-écologique de la production et de la transformation du cajou en Afrique : Problématique–Acquis scientifiques et technologiques–Perspectives, Bassam, Côte d’Ivoire, 26-28 octobre 2017.

4.         FIRCA. Rapport annual. 2022. Available online: https://firca.ci/ressources/ publications/rapports-annuels-et-bilans/(Accessed  on    10 June 2024).

5.         MINADER. Evaluation environnnementale, sociale et stratégique (EESS) de la zone agro- industrielle de Korhogo. Projet d’appui à la compétitivité de la chaîne de valeur de l’anacarde en Côte d’Ivoire. World Bank Documents. 2017, 13p. Available online: https://documents.worldbank.org › curated › pdf. (Accessed on 18 January 2022).

6.         Koffi S.Y.; Oura, K.R. Les facteurs de l’adoption de l’anacarde dans le basin cotonnier de Côte d’Ivoire. Cah. Agric.  2019, 28 (24), 8. https://doi.org/ 10.1051/cagri/2019025.

7.         Meier, U.; Bleiholder, H.; Buhr, L, Feller, C., Hack, H.; He, B. M., Weber, E. Use of the extended BBCH scale- general for the descriptions of the growth stages of mono and dicotyledonous weed species. Weed Res. 008, 37(6), 41– 52. https://doi.org/10.1046/j.1365- 3180.1997.d01-70.x

8.         Adiga, J.D.; Muralidhara, B.M.; Preethi, P.; Savadi, S. Phenological growth stages of the cashew tree (Anacardium occidentale L.) according to the extended BBCH scale. Ann. Appl. Biol. 2019, 175, 246–252. https://doi.org/10.1111/ aab.12526.

9.         Jestin, A. Modélisation du développement et de la phénologie du manguier. Master professionnel, Université Claude Bernard de Lyon 1, 2013.

10.      Hack, H.; Bleiholder, H.; Buhr, L.; Meier, U.; Schnock-Fricke, U.; Weber, E.; Witzenberger, A. Ein-heitliche codierung der phãnologischen entwicklun- gsstadien mono-und dikotyler pflanze n-erweiterte BBCH-Skala, Allgemein . Nachrichtenbl Deut Pflanzenschutzd. 1992, 44, 265-270.

11.      Niemenak, N.; Cilas, C.; Rohsius, C.; Bleiholder, H.; Meier, U.; Lieberei, R. Phenological growth stages of cacao plants (Theobroma sp.): codification and description according to the BBCH scale. Annals of Appl. Biol. 2010, 156, 13-24. https://doi.org/10.1111/j.1744-7348.2009.00356.x.

12.      Lorez, D.H.; Eichhorn, K. W.; Bleiholder, H.; Klose, R.; Meier, U.; Weber, E. Growth stages of the grapevine: Phenological growth stages of the grapevine (Vitis vinifera L. ssp. vinifera) Codes and descriptions according to the extended BBCH scale. Aus. J. Grape Wine Res. 1995, 1, 100-103. https://doi. org/10.1111/j.1755- 0238.1995.tb00085.x.

13.      Agustí, M.; Zaragoza, S.; Bleiholder, H.; Buhr, L., Hack, H.; Klose, R.; Stau, R. Adaptation of the BBCH scale for the description of citrus fruits' phenological stages. Fruits. 1997, 52, 287-295.

14.      Salazar, D.M.; Melgarejo, P.; Martínez, R.; Martínez, J.J.; Hernández,  F.; Burguera, M. Phenological stages of the guava tree (Psidium guajava L.). Scientia Hort. 2006, 108(2), 157-161. https://doi.org/10.1016/j.scienta. 2006.01.022.

15.      Delgado, P.H.; Aranguren, M.; Reig, C.; Galvan, D.F.; Mesejo, C.; Fuentes A.M.; Agusti, M.  Phenological growth stages of mango (Mangifera indica L.) according to the BBCH scale. Scientia Hort. 2011, 130 (3), 536-540. https://doi.org/10.1016/j.scienta.2011.07.027.

16.      Coulibaly, T.J.H. Répartition spatiale, gestion et exploitation des eaux souterraines : cas du département de Katiola, région des savanes de Côte d’Ivoire. Thèse de doctorat, Université de Paris Est, France, 2009.

17.      Pavithran, K.; Ravindranathan, P.P.  Studies on floral biology in cashew, (Anacardium occidentale L.). J. Plant. Crops. 1974, 2, 32-33.

18.      Masawe, P.A.L.; Kapinga, F.A.;   Caligari, P.D.S. Variation in the period of nut harvesting among cashew trees in southern Tanzania. In Proceeding of the second international cashew conference. Kampala, Uganda, 2010.

19.      N'Da, H.A.; Akanvou, L.; Kouakou, C.K. Gestion locale de la diversité variétale du maïs (Zea mays L.) violet par les Tagouana au Centre-Nord de la Côte d'Ivoire. Int. J. Biol. Chem. Sci. 2013, 7(5), 2058-2068.