Dwarfism and grafting compatibility induced by ‘flying dragon’ rootstock for different citrus cultivars

ABSTRACT

The rootstock Poncirus trifoliata var. monstrosa flying dragon (FD) induces dwarfism to citrus trees. Dwarfism provides several positive aspects: allows dense planting, reduces the pruning frequency, improves productivity efficiency, and makes cultural practices easier. Evaluating the compatibility of the rootstock with different scion varieties is crucial for recommending this rootstock and requires many years of field observations. The aim of this investigation was to evaluate the vigor and graft compatibility of Citrus × sinensis L. Osbeck and Citrus × latifolia Tanaka grafted onto FD. The experimental was a randomized block design, with five treatments, four replications, and each plot consisting of one tree. The cultivar Tahiti acid lime IAC-5 and Seleta, Lima, Bahia, and Folha Murcha oranges were the evaluated plants. Biometric measurements of canopy and graft incompatibility were assessed, and viables spacing were estimated. No signs of incompatibility were observed in any graft combination. After 12.5 years, FD induced dwarfism in all evaluated cultivars, but not to Tahiti acid lime. In the edaphoclimatic conditions of North Fluminense, we suggest planting densities of 511, 1,387, 1,486, 792 and 1,644 plants.ha^-1 to Tahiti, Seleta, Lima, Bahia, and Folha Murcha oranges trees, respectively, when these are grafted onto the FD.

Key words
Poncirus trifoliata var. monstrosa; Citrus sinensis (L.) Osbeck; Citrus × latifolia Tanaka ; late incompatibility; high planting density

INTRODUCTION

Brazil has been the world’s largest orange producer, with a production of 16 million tons in 2022 (FAO 2021). In that harvest, the production value reached R$ 16.9 billion, covering a harvested area of 570.9 thousand hectares (IBGE 2021). The most cultivated orange varieties in Brazil are Pera, Valência, Natal, and Hamlin, primarily destined for juice industries. Other orange varieties grown in Brazil, as acid limes, are aimed at the fresh fruit market and have more regional importance (Lima et al. 2014).

Citrus, like other fruit tree species, are vegetatively propagated through grafting (Hayashi et al. 2012). Despite the numerous scion cultivars available, the range of rootstock cultivars is limited. According to Conceição et al. (2019), the Rangpur lime (Citrus × limonia Osbeck) and Swingle citrumelo (Citrus × paradisii Macfad. cv. Duncan × Poncirus trifoliata (L.) Raf.) represented 34 and 45%, respectively, of the rootstocks used for citrus seedling production in São Paulo in 2017, highlighting the genetic vulnerability of our orchards.

Several factors influence the size of citrus plants, including the rootstock used, plant variety, soil and climate conditions, cultural management practices, and the phytosanitary status of the plants (Stuchi 1994). Effective control of citrus plant growth can be achieved through various strategies, with the use of dwarfing rootstocks being one of the most effective (Carvalho et al. 2018).

Regarding the major phytosanitary problems affecting citrus cultivation in Brazil, the highly limiting disease is currently Huanglongbing (HLB), caused by the bacterium Candidatus Liberibacter asiaticus (C Las) and transmitted by the Asian citrus psyllid Diaphorina citri. This disease has led to changes in traditional cultivation areas, with new orchards being implemented with denser planting and the use of more suitable rootstocks for this cultivation system (Gonzatto et al. 2022).

Dwarfing rootstocks are desirable for implementing denser orchards. This approach contributes to improving yield and net profits, especially during the initial stages of orchard growth, allowing for the cultivation of more plants per area than traditional planting systems (Ladaniya et al. 2021). Additionally, denser plantings during the HLB epidemic have been also associated with lower disease incidence and greater economic viability (Moreira et al. 2019).

The rootstock P. trifoliata var. monstrosa flying dragon (FD) induces dwarfism in the grafted scions, which reach a maximum height between 2.5 and 3 m after growth stabilization, occurring approximately 10 years after planting (Mademba-Sy et al. 2012). However, its recommendation is currently limited to the Tahiti acid lime, clone IAC-5, as there are not enough studies to recommend it as a rootstock for other cultivars (Stuchi and Silva 2005).

Some theories have been proposed to explain the ability of FD to induce dwarfing in scions, such as those proposed by Martínez-Alcántara et al. (2013) and Carvalho et al. (2018). They suggest that this characteristic is linked to the small number of vessels present in the xylem region, which induces low hydraulic conductivity in this rootstock. The restriction in the transport speed within the xylem could be associated with reduced translocation of water and hormones to the shoots, thus contributing to dwarfing. Carvalho et al. (2018) further assert that the anatomical differences leading to dwarfing may also result in graft incompatibility.

Evaluating graft compatibility between various scions and FD is crucial for recommending this rootstock for other cultivars and requires many years of field observations. This is necessary because late incompatibility can occur at any stage of the reproductive cycle. The formation of a functional graft involves complex processes, including callusing between the scion and rootstock and the development of a cambium, which forms functional vascular connections between the aerial and root systems. Good graft compatibility results in the healthy growth of the combined plant, allowing for the commercial exploitation of an orchard without the manifestation of symptoms such as hypertrophies, gum formation, or the presence of necrotic lines in the graft region (Carvalho et al. 2018, Pompeu Júnior et al. 2005).

Similarly, choosing to space that induces greater productivity is critical in establishing orchards. One of the most accurate methods for defining spacing is to evaluate, under planned planting conditions, the vigor of older plantings under similar soil, climate, and management conditions. The objectives of this study were to establish spacing estimates and to assay the compatibility of sweet orange (Citrus × sinensis L. Osbeck) and Tahiti acid lime (IAC-5) (Citrus × latifolia Tanaka) grafted onto the FD rootstock, 12.5 years after planting, under irrigation and the edaphoclimatic conditions of the Northern Fluminense region.

In this context, the hypothesis was that the rootstock P. trifoliata var. monstrosa FD was compatible with different citrus varieties, inducing dwarfing and providing greater productive efficiency without causing graft incompatibility. The objective of the study was to evaluate the vigor and graft compatibility of sweet orange (Citrus × sinensis L. Osbeck) and Tahiti acid lime (Citrus × latifolia Tanaka) grafted onto the FD rootstock.

MATERIAL AND METHODS

The experimental design used was a completely randomized block with five treatments, four replications, and each plot consisting of one plant. The FD rootstock was used for all scions. The scions used were Tahiti acid lime, clone IAC-5, and the sweet oranges Seleta, Lima, Bahia, and Folha Murcha. The orchard was established with the spacing of 6 × 3 m under localized irrigation with two drippers per plant and fertilized according to the recommendations of Ribeiro et al. (1999). Biometric evaluations were performed at 12.5 years after planting and consisted of measure of plant height, canopy diameter in the row (CDR) and between rows (CDBR) of planting, stem diameter at the grafting region (DGR), 15 cm above (DGRA), and below (DGRB) of union grafting between both parts and canopy volume, which was obtained by applying Eq. 1 (Zekri et al. 2003), expressed in m³:

$VC=\frac{\pi }{6}\times H\times CDR\times CDBR$ (1)

where: CV: average canopy volume; H: plant height; CDR: canopy diameter in the row; CDBR: canopy diameter between rows.

The ideal distance was also calculated, being a population of plants per hectare estimated for each graft, using Eq. 2a, in which 10,000 m² is the area equivalent to 1 hectare, and A is the theoretical area:

$A=0,85\times CDR\times (CDBR+2)\frac{10,000m^2}{A}$ (2)

where: CDR the canopy diameter in the planting row; CDBR: the canopy diameter between rows.

For Eq. 2, it is assumed that there is a 15% overlap of branches in the row and that there is a distance of 2 m for carrying out cultural practices (Carvalho et al. 2022a). Rectangular cuts (windows) were also made in the trunks of the plants to expose the vascular cambium for graft compatibility evaluation. The data were subjected to analysis of variance, and the means of the treatments were compared by Tukey’s test considering p > 0.05.

RESULTS

At 12.5 years after planting, Tahiti acid lime was the cultivar that differed from the others for all evaluated traits (Fig. 1). Only for the stem diameters at the grafting region (Fig. 1d) and above (Fig. 1e) and below (Fig. 1f) the grafting region, the cultivar showed the lowest averages.

Figure 1
(a) Height (cm); (b) canopy diameter in the planting row (CDR) (cm); (c) canopy diameter between planting rows (CDBR) (cm); (d) stem diameter at the grafting region (DGR) (cm); (e) stem diameter below the grafting region (DGRA) (cm); (f) stem diameter above the grafting region (DGBR) (cm); and (g) canopy volume (m³) for different cultivars of orange trees grafted onto the flying dragon rootstock.

Carvalho et al. (2018), when evaluating the same orchard at 3.5 years old, observed that the Tahiti acid lime was the plant with the tallest height, volume, and canopy diameter in the row. At that time, the younger plants were still likely to reach higher canopy volumes. Upon reaching maturity, Tahiti acid lime demonstrated to be the most vigorous cultivar when grafted onto the dwarfing FD rootstock, confirmand this tendency initial at 3.5 years old.

Regarding the orange cultivars, the Bahia orange stood out from the others for all the evaluated variables.

The data regarding the average heights shown in Fig. 1a, for the orange trees grafted onto the FD rootstock, align with the pattern mentioned by Mademba-Sy et al. (2012). Thus, the FD rootstock induced dwarfism in the orange tree canopies, but not in the Tahiti acid lime, which reached a height of 2.9 m.

Azevedo et al. (2020) evaluated different planting systems for the Tahiti acid lime grafted onto FD, in high planting density (1,157 trees.ha^-1). In the research, they stated that the canopy volume of the Tahiti acid lime was still considered small, at 5-year-old orchard. However, after applying the formulas presented for this purpose, the present study indicated, at 12.5 years of age, a spacing of 3.3 × 6 m for Tahiti acid lime, allowing a planting density of 512 trees.ha^-1. These results indicated that planting density for Tahiti acid lime must be based on studies over 10 years of age. Spacing of 1.75 × 4.12 m for Seleta, 1.74 × 3.87 m for Lima, 2.66 × 4.82 m for Bahia and 1.51 × 4.03 for Folha Murcha cultivars, under the edaphoclimatic conditions of the Northern Fluminense, were estimated, making it possible to suggest higher density for new orchards with oranges cultivars, ranging from 788 to 1,636 plants per hectare, depending on the canopy used. Commercially, the most used spacings for orange trees are about 6 m between rows and 3 m within rows (Sampaio et al. 2016, Amorim et al. 2018, Carvalho et al. 2018).

For the canopy/rootstock relationship, it was estimated that a higher grafting affinity would result in similar trunk diameters for canopy and rootstock. When this greater affinity occured, the values of the relationship between canopy diameter and rootstock approached 1. The relationship between the diameter of the scion trunk and the rootstock, which is obtained by dividing DGRA by DGRB, must be correlated to the good performance of the grafted plant, this correlation being established through the balance in sap circulation (Nogueira Filho et al. 2010). For the evaluated combinations, the following results were obtained for the relationship of different canopies on the FD rootstock: Tahiti, 0.65; Seleta, 0.69; Lima, 0.63; Bahia, 0.55; e Folha Murcha, 0.58. The diameter of the canopy trunk is generally smaller than that of the rootstock, in the case of trifoliate rootstocks or their hybrids.

All canopy/rootstock combinations, in the 20 evaluated plants, showed no visual signs of incompatibility at 12.5 years of age (Fig. 2). No lines or depressions were observed. However, a more yellowish sap and tighter bark were observed in the grafting region in some trees. As a characteristic, the FD does not shed its shell easily. When forcing the windows open with a pocketknife, the situations mentioned above arise. The time between opening the windows and taking the photograph may have allowed a certain degree of oxidation of the material.

Figure 2
Grafting region of the combinations: (a) Tahiti; (b) Seleta; (c) Lima; (d) Folha Murcha; (e) Bahia, on the flying dragon rootstock.

Incompatibility in citrus rootstocks was studied by Carvalho et al. (2018), who used FD and Rangpur lime rootstocks with five commercial scions under the same edaphoclimatic conditions as in the present study and observed visual symptoms of incompatibility between the Pera orange grafted onto FD, identified 64 months after planting. The FD rootstock showed visually more clustered vascular elements with smaller diameters compared to the vascular elements of the Pera orange and Rangpur lime, which were more like each other. It was also noted that the Bahia orange exhibited good anatomical plasticity, adjusting more efficiently to the rootstocks. The size and frequency of the vessels, as well as the arrangement and size of the cambial zone, are related to dwarfism and graft incompatibility. This may explain the better growth performance observed in the Bahia orange at 12.5 years of cultivation compared to the other orange varieties.

There is still no data on graft compatibility between FD and Folha Murcha orange cultivar. However, this scion variety has been widely used due to its tolerance to HLB. In a study by Carvalho et al. (2022b), which aimed to evaluate various horticultural characteristics of 19 late-season sweet orange selections grafted onto Rangpur lime under endemic conditions of citrus canker and HLB, it was found that Folha Murcha had the lowest disease incidence. In the present study, this scion remains viable for cultivation after 12.5 years when grafted onto FD. The smaller size and, if confirmed, its greater resistance to HLB could result in a desirable combination for planting in higher densities. The Folha Murcha orange can be used for industry and fresh fruit markets, and, in the context of establishing new denser orchards, it could be an interesting option.

Rectangular cuts at the grafting point did not show ruptures in the canopy/rootstock connection (Fig. 2d). The phloem sap coloration was more yellowish, which may indicate incipient incompatibility, but so far has not resulted in external symptoms such as plant depletion, tip dieback, or other signs of vigor loss. Therefore, further observation time and other studies focusing on the FD and Folha Murcha combination are recommended.

Among the orange varieties, the Bahia orange presented higher values in biometric characteristics, when compared to other combinations, drawing attention due to its better performance over the years when grafted onto FD. Portella et al. (2015), when evaluating this combination and four other scions after three years of planting, found that Bahia was the scion with the shortest height. However, at 5.5 years when compared with four other scions, it only had a significant difference for Tahiti acid lime (Carvalho et al. 2018). This cultivar also exhibited the same symptoms as Folha Murcha when rectangular cuts were made in the grafting region (Fig. 2E). It is still possible that incompatibility symptoms may arise in the future in the orchard. Therefore, the continuation of studies on the orchard and the monitoring of performance in the field of different canopy combinations are important for the continuity of successful citrus cultivation in Brazil.

Based on the evaluated indicators, 12 years after planting, it can be concluded that all the combinations are compatible until now, and the dwarfism induced by the FD rootstock on the orange tree canopies is confirmed, but not for Tahiti acid lime.

CONCLUSION

Based on the results after 12.5 years of cultivation, the initial hypothesis was partially confirmed. The P. trifoliata var. monstrosa FD rootstock proved to be compatible with all the evaluated cultivars, showing no visible signs of graft incompatibility, as observed in the rectangular cuts at the grafting point. No external signs of plant depletion or vigor loss were recorded, supporting the compatibility of these combinations thus far. Additionally, FD successfully induced dwarfing in all sweet orange (Citrus × sinensis) varieties, as hypothesized, except for Tahiti acid lime (Citrus × latifolia), which maintained a more vigorous growth and exceeded 2.5 m in height, contradicting the dwarfing trend. In this case, it is not recommended for high-density cultivation.

Among the evaluated cultivars, the Bahia orange tree is the one that shows the best growth characteristics and absence of graft incompatibility.

These findings indicate that FD is effective in inducing dwarfing in sweet orange trees, enabling the possibility of high-density plantings, with recommended ranging from 792 to 1,644 trees per hectare, depending on the variety.

The absence of visible signs of incompatibility suggests a stable scion-rootstock relationship during the evaluated period. However, the observation of yellowish sap and tighter bark in some trees, although not causing depletion, highlights the need for continuous monitoring to ensure the longevity of the orchards.

ACKNOWLEDGMENTS

We would like to thank Universidade Estadual do Norte Fluminense Darcy Ribeiro for the provision of space for the execution of the experiment.

• How to cite: Silva, R. M. R., Marinho, C. S., Galvão, S. P., Santos, R. F. and Silva, A. E. (2025). Dwarfism and grafting compatibility induced by ‘flying dragon’ rootstock for different citrus cultivars. Bragantia, 84, e20240236. https://doi.org/10.1590/1678-4499.20240236
• FUNDING
  Not applicable.

DATA AVAILABILITY STATEMENT

The data used and/or analyzed during the course of this study are available upon reasonable request to the corresponding author.

REFERENCES

• Amorim, M. D. S., Girardi, E. A., França, N. D. O., Gesteira, A. D. S., Soares Filho, W. D. S. and Passos, O. S. (2018). Initial performance of alternative citrus scion and rootstock combinations on the northern coast of the state of Bahia, Brazil. Revista Brasileira de Fruticultura, 40, e-480. https://doi.org/10.1590/0100-29452018480
  » https://doi.org/10.1590/0100-29452018480
• Azevedo, F. A., Almeida, R. F., Martinelli, R., Prospero, A. G., Licerre, R., Conceiçao, P. M., Arantes, A. C. C., Dovis, V. L., Boaretto, R. M. and Mattos Jr., D. (2020). No-tillage and high-density planting for Tahiti acid lime grafted onto Flying dragon trifoliate orange. Frontiers Sustainable Food Systems, 4, 108. https://doi.org/10.3389/fsufs.2020.00108
  » https://doi.org/10.3389/fsufs.2020.00108
• Carvalho, D. U., Leite Junior, R. P., Yada, I. F. U. and Tazima, Z. H. (2022a). Trifoliate orange-related rootstocks enhance the horticultural performance of ‘Shamouti’Sweet orange under humid subtropical condition. Agriculture, 12, 1782. https://doi.org/10.3390/agriculture12111782
  » https://doi.org/10.3390/agriculture12111782
• Carvalho, D. U., Neves, C. S. V. J., da Cruz, M. A., Longhi, T. V., Behlau, F., de Carvalho, S. A. and Leite Junior, R. P. (2022b). Late-season sweet orange selections under huanglongbing and citrus canker endemic conditions in the Brazilian humid subtropical region. Frontiers in Plant Science, 13, 915889. https://doi.org/10.3389/fpls.2022.915889
  » https://doi.org/10.3389/fpls.2022.915889
• Carvalho, W. S., Marinho, C. S., Arantes, M. B. D. S., Campbell, G., Amaral, B. D. and da Cunha, M. (2018). Agronomic and anatomical indicators of dwarfism and graft incompatibility in citrus plants. Journal of Agricultural Science, 10, 263. https://doi.org/10.5539/jas.v10n9p263
  » https://doi.org/10.5539/jas.v10n9p263
• Conceição, P. M., Azevedo, A., Ecker, G. V. and Cristofani, M. (2019). Physiological quality of citrandarins, Poncirus trifoliata and Sunki mandarin seeds. Comunicata Scientiae, 10, 461-466. https://doi.org/10.14295/cs.v10i4.3138
  » https://doi.org/10.14295/cs.v10i4.3138
• [FAO] Food and Agriculture Organization of the United Nations (2021). Crops and livestock products: annual statistics. FAO. Available at: https://www.fao.org/faostat/en/#data/QCL/visualize Accessed in: May 2024.
  » https://www.fao.org/faostat/en/#data/QCL/visualize
• Gonzatto, M. P., Griebeler, S. R. and Schwarz, S. F. (2022). Porta-enxertos anões para pomares cítricos de alta densidade. In I. Kahramanoglu and C. P. Wan (Eds.). Fruit Industry (p. 1-16). London: IntechOpen.
• Hayashi, S., Girardi, E. A., Silva, S. R., Stuchi, E. S. and Cantuarias-Avilés, T. (2012). Avaliação de fita fotodegradável para enxertia em mudas de citros. Revista Brasileira de Fruticultura, 34, 641-645. https://doi.org/10.1590/S0100-29452012000200042
  » https://doi.org/10.1590/S0100-29452012000200042
• [IBGE] Instituto Brasileiro de Geografia e Estatística (2021). PAM - Produção Agrícola Municipal 2021. IBGE. Available at: https://www.ibge.gov.br/estatisticas/economicas/agricultura-e-pecuaria/9117-producao-agricola-municipal-culturas-temporarias-e permanentes.html?edicao=34923&t=destaques. Accessed in: May 2024.
  » https://www.ibge.gov.br/estatisticas/economicas/agricultura-e-pecuaria/9117-producao-agricola-municipal-culturas-temporarias-e permanentes.html?edicao=34923&t=destaques
• Ladaniya, M., Marathe, R., Murkute, A., Huchche, A., Das, A., George, A. and Kolwadkar, J. (2021). Response of Nagpur mandarin (Citrus reticulata Blanco) to high density planting systems. Scientific Reports, 11, 10845. https://doi.org/10.1038/s41598-021-89221-4
  » https://doi.org/10.1038/s41598-021-89221-4
• Lima, C. F., Marinho, C. S., Costa, E. S. and Amaral, C. O. (2014). Qualidade dos frutos e eficiência produtiva da laranjeira ‘Lima’enxertada sobre ‘Trifoliata’, em cultivo irrigado. Revista Brasileira de Ciências Agrárias, 9, 401-405. https://doi.org/10.5039/agraria.v9i3a4433
  » https://doi.org/10.5039/agraria.v9i3a4433
• Mademba-Sy, F., Lemerre-Desprez, Z. and Lebegin, S. (2012). Use of Flying Dragon trifoliate orange as dwarfing rootstock for citrus under tropical climatic conditions. Hort Science, 47. https://doi.org/10.21273/HORTSCI.47.1.11
  » https://doi.org/10.21273/HORTSCI.47.1.11
• Martínez-Alcántara, B., Rodriguez-Gamir, J.Martínez-Cuenca, M. R., Iglesias, D. J., Primo-Millo, E. and Forner-Giner, M. A. (2013). Relationship between hydraulic conductance and citrus dwarfing by the Flying Dragon rootstock (Poncirus trifoliata L. Raft var. monstruosa). Trees, 27, 629-638. https://link.springer.com/article/10.1007/s00468-012-0817-1
  » https://link.springer.com/article/10.1007/s00468-012-0817-1
• Moreira, A. S., Stuchi, E. S., Silva, P. R. B., Bassanezi, R. B., Girardi, E. A. and Laranjeira, F. F. (2019). Could tree density play a role in managing Citrus Huanglongbing epidemics? Tropical Plant Pathology, 44, 268-274. https://doi.org/10.1007/s40858-019-00284-1
  » https://doi.org/10.1007/s40858-019-00284-1
• Nogueira Filho, G. C., Roncatto, G., Ruggiero, C., Oliveira, J. C. D. and Malheiros, E. B. (2010). Desenvolvimento e produção das plantas de maracujazeiro-amarelo produzidas por enxertia hipocotiledonar sobre seis porta-enxertos. Revista Brasileira de Fruticultura, 32, 535-543. https://doi.org/10.1590/S0100-29452010005000071
  » https://doi.org/10.1590/S0100-29452010005000071
• Pompeu Júnior, J., Mattos Júnior, D., De Negri, J. D. and Pio, R. M. (2005). Porta-enxertos. In J. Pompeu Júnior, D. Mattos Júnior, J. D. De Negri and R. M. Pio (Eds.). Citros (p. 61-104). Campinas: Instituto Agronômico e Fundag.
• Portella, C. R., Marinho, C. S., Amaral, B. D., Carvalho, W. S. G., Campos, G. S., Silva, M. P. S. D. and Sousa, M. C. D. (2015). Desempenho de cultivares de citros enxertadas sobre o trifoliateiro ‘Flying Dragon’ e limoeiro ‘Cravo’ em fase de formação do pomar. Bragantia, 75, 70-75. https://doi.org/10.1590/1678-4499.267
  » https://doi.org/10.1590/1678-4499.267
• Ribeiro, A. C., Guimarães, P. T. G. and Alvarez, V. H. (Eds.) (1999). Recomendações para o uso de corretivos e fertilizantes em Minas Gerais: 5ª Aproximação. Viçosa: CFSEMG.
• Sampaio, A. H. R., Coelho Filho, M. A., Souza, L. D., Brito, R. B. F. and Silva, R. O. D. (2016). Produtividade e qualidade de laranjeira doce ‘Pera’ enxertada em diferentes porta-enxertos em regime de sequeiro. Revista Brasileira de Fruticultura, 38, e-770.
• Stuchi, E. S. (1994). Controle do tamanho das plantas cítricas. Laranja, 15, 295-342.
• Stuchi, E. S. and Silva, S. R. (2005). Plantio adensado da limeira-ácida Tahiti. Cruz das Almas: Embrapa Mandioca e Fruticultura. (Citros em Foco, 29.)
• Zekri, M., Obreza, T. A. and Koo, R. (2003). Irrigation, nutrition, and citrus fruit quality. SL 207, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. https://doi.org/10.32473/edis-ss426-2003
  » https://doi.org/10.32473/edis-ss426-2003

• Section Editor:
  Gabriel Constantino Blain https://orcid.org/0000-0001-8832-7734

Publication Dates

• Publication in this collection
  03 Feb 2025
• Date of issue
  2025

History

• Received
  16 Oct 2024
• Accepted
  10 Dec 2024