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Cuban Journal of Agricultural Science

versão impressa ISSN 0864-0408versão On-line ISSN 2079-3480

Cuban J. Agric. Sci. vol.55 no.3 Mayabeque jul.-set. 2021  Epub 01-Set-2021

 

Review Article

Gamic seed production of Tithonia diversifolia Hemsl.) A. Gray. sowing and establishment

C. Padilla Corrales1  * 
http://orcid.org/0000-0002-6794-8694

Idalmis Rodríguez García1 
http://orcid.org/0000-0001-5897-5431

1Instituto de Ciencia Animal, Apartado Postal 24, San José de las Lajas. Mayabeque, Cuba

Abstract

This review aims to spread the advances in the production of gamic seed of Tithonia diversifolia Hemsl.) A. Gray. and the establishment in this way. The germination of this species is reported, as well as the ways to increase it through dormancy detection, seed conservation, types of substrates and their performance under laboratory and nursery conditions, as well as the variables related to the morphostructure of seedlings until transplantation. It is shown that germination percentages between 50 and 90 % can be reached when the seeds are harvested at the optimum moment and treatments that favor viability and germination are applied. The integral agronomic management allowed defining the best harvest time and the effects on different practices that allow the appearance of uniform flowering flows and obtaining yields of the order of 20-30 kg of pure germinable seed (PGS). Results are discussed and reported on the real possibility of achieving satisfactory establishments and acceptable biomass production when different practices are used to protect gamic seeds with plant and organic wastes. It is showed for the first time, the advantages of the sowings by gamic seed in relation to the plantations by cuttings and in bags for the forage yield (11.68 vs 9.48 and 9.92 t DM.ha-1) and for the populations (10.55 vs 5.88 and 10.88 plants.m-2) respectively, in the establishment cut. The advances made allow the promotion of seed production and achieve a greater introduction and generalization of this species, which in turn can contribute to an increase in food production.

Key words: Germination; Tithonia diversifolia; pure germinable seed (PGS); establishment; production and gamic reproduction

INTRODUCTION

Tithonia diversifolia Hemsl.) A. Gray stands out for its high ecological and productive plasticity, which contributes to be considered the most accepted protein plant by farmers in Cuba and other regions of the world (Paniagua-Hernández et al. 2020). New researches, related to the impact of climate change on the presence and potential distribution of Tithonia, reveal that for all the evaluated scenarios the effect would be beneficial, so there are not affectations for this crop and they can continue to play the role it represents in animal feeding (Durant et al. 2020).

One of the main limitations for the extension of this species is that the propagation is carried out almost 100 % through the use of cuttings, which are easy to acquire from other crops, but it should be noted that this type of propagation have some difficulties such as the cost of transportation and storage that can only be done for short periods, without affecting the quality of cuttings (Sánchez et al. 2014). Solving the previous problem constituted a challenge for the scientific community in the last 10 years, which implied developing comprehensive researchers that would optimize the germination and conservation processes of the gamic seed. As well as, to establish the scientific and technical bases for seeds production and the establishment of this plant in this way in Cuba and other regions of the world.

Faced with the problem and the challenge exposed, the purpose of this review is to make available to farmers, managers, researchers, professors and students from the livestock sector, a document where the advances in the production of gamic seed were collected and analyzed and in the establishment in this way.

ANTECEDENTS

The Tithonia genus belongs to Asteraceae family, Tithonia diversifolia Hemsl.) A. Gray. is one of the twelve species that comprise this genus which are native to Central America. However, there is evidence of high levels of genetic diversity in all populations from other continents such as China (Jing et al. 2012) and Africa, where most of the researches carried out shows this (Etejere and Oleyinka 2014 and Obiakara and Forcade 2018). In general, the approach of these researchers, in both regions, is mainly aimed at evaluating ecological and dispersal aspects.

Similarly, in the American continent, the genetic diversity of T. diversifolia and its great capacity for adaptation and survival are evaluated (Rivera 2020). However, most of the researches have mainly focused on its capacity to produce biomass, evaluate its quality and fundamentally its use in animal feeding.

There is very little information on the characterization of different specimens, materials or cultivars of this species. In Cuba, since 2006 (Ruíz et al. 2017), the contrasting characteristics were determined, in terms of morphological traits and germination percentage, of a group of Tithonia materials collected in different edaphoclimatic regions of the country (29 materials from the central-western zone, 2006 and 52 materials from the central-eastern zone, 2015).

Inayat (2009) refers to the presence of five materials in the national herbarium of Quito (provenance from the northwestern Pichincha and in Napo province) and in Mexico Del Val et al. (2014) carried out a study of genetic diversity with molecular markers type SSR (Simple Sequence Repeats) and characterized T. diversifolia plants from different areas of Michoacán and Mexico City and others found in the plant germplasm bank of Fundación Produce Michoacán A. C, these authors obtained 11 ADN samples that are preserved in the Molecular Biology Laboratory from the Technological Institute of Tlajomulco, Jalisco.

Holguín et al. (2015) in Colombia, evaluated the response in the forages production of 44 introductions of T. diversifolia, from several localities in the central west of the country, which are established in a collection at the Centro Experimental Universidad Nacional Palmira headquarters (CEUNP) Candelaria.

Recently, Rivera (2020) reports the genetic diversity of this shrub in materials collected in Colombia and Mexico, this author evaluated 31 populations and determined differences in the evaluation of reproductive aspects between genotypes except for the drying time of achenes and the percentage of rudimentary seeds.

PROPAGATION EXPERIENCES OF TITHONIA DIVERSIFOLIA BY GAMIC SEED

The first propagation experiences of Tithonia diversifolia (tree marigold) by gamic seed were obtained, in Colombia, by spreading the branches with flowers or peduncles that have lost their petals, on an organic substrate under a polyshade as protection against solar radiation and the raindrops. The obtained seedlings are carefully selected, either for transplanting them into nursery bags or for sowing them directly in well-prepared soils (Galindo et al. 2011 and Romero et al. 2014).

Subsequently, different researchers related to the characterization of gamic seed were carried out and studies performed in Brazil (Saavedra, 2016) highlighted the importance of knowing how phenology and physiology influence on the formation of seeds and their quality. However, the obtained results so far in this regard have not considered comprehensive studies to determine how phenological changes affect floral structures over time and in the formation and physiological maturation of seeds and define a technology for obtaining of quality seed that favors its commercialization.

The previous was a great challenge for the scientific community to achieve an efficient technology in the production of T. diversifolia seed by gamic way. In this sense, different researchers (Santos-Gally et al. 2017, Padilla et al. 2018, Mattar et al. 2019 and Santos-Gally et al. 2019) contribute to the knowledge of biology and the factors that influence on the percentage of germination of gamic seed and constitute an important source of information on the aspects covered in this review.

BOTANICAL CHARACTERIZATION OF THE REPRODUCTIVE STRUCTURE OF TITHONIA

Researchers aimed at promoting adequate commercial seed production of this plant require broadening the biological knowledge of the inflorescence and the formation of the achene. The botanical characterization of T. diversifolia inflorescences constitutes a topic widely addressed by different authors (Wang et al. 2008, Pérez et al. 2009, González-Castillo et al. 2014 and Saveedra 2016). However, there is little scientific knowledge of the physiological and reproductive performance of Tithonia, which limits the advance in its domestication as a multipurpose species.

Studies on the cytogenetics and the characterization of the reproductive strategy of this species (Alcorcés et al. 2007) show that between 15 and 26 % of empty fruit and 50 and 62 % of non-viable seed are produced in achenes; only 18 and 22 % of the produced seed has the ability to germinate. The low germination percentage (20 %) of the achenes is associated with the high percentage of sterile pollen (65 %) lacking sperm nucleus, which is attributed to the low sexual reproduction that it have. Other reasons for the sterility of pollen are related to the problems that occur in the meiotic division, where lagging chromosomes are observed in anaphase I, avoiding the dragging of chromosomes towards the poles, which can misalign a chromosome, generating negative signals that identify the cell (Guerra et al. 2007).

According to Santos-Gally et al. (2020) the heteromorphism in the seed heads of T. diversifolia is mainly characterized by differences between central and peripheral achenes, which could represent a strategy for this species to adapt to adverse environmental conditions. These authors point out that central achenes have edges (potentially associated with zoocoria dispersion), weak latency and higher rate and germination success, however, peripheral achenes lack structures associated with dispersal and have a lower germination rate and success.

According to La Duke (1980) the T. diversifolia seed heads have around 80 to 120 tubular flowers, which in this case are the ones that form the seeds or achenes. Some of the values reported in the literature are in these ranges, such is the case of the studies by Silva et al. (1990) reporting 89.9 seeds. seed heads-1 in Brazil. Etejere and Olayinka (2014 and 2015) in Nigeria found lower values of 32-62 seeds heads-1 and in Cuba Rodríguez et al. (2021) determined, in three evaluated materials (10, 23 and 25), values of 63.52, 56.63 and 75.87 seeds. seed heads-1, respectively.

However, in other regions higher values are reported. In China, Wang et al. (2004) determined between 164.20 and 231.00 seeds. seed heads-1 and in Nigeria, Muoghalu and Chuba (2005) and Muoghalu (2008) show values of 179.70 and between 136 - 144 seeds. seed heads-1, respectively. On the other hand, Mattar et al. (2019) in Brazil show values higher than 189.80 seeds.

The above shows the complexity of the gamic seed production of this species. Similarly, the indicators reported on the weight of 1000 seeds and the number of seedlings per kg of seed (table 1) shows great variability in the literature.

Table 1 Results of the weight of 1000 seeds and number of seeds per kilogram of seeds found by different authors 

Country Weight of 1000 seeds, g Estimated number of seeds per kg of seed Authors
Colombia - 17000.00 Romero et al. (2014)
7.35 136054.00 Gallego- Castro (2016)
- 100000.00 Cortez et al. (2019)
Costa de Marfil 2.40 409836.06 Tiebre et al. (2012)
Nigeria

  • 6.42

  • 7.50

  • 155763.00

  • 133333.00

Etejere y Olayinka (2014)
México 1.00 1000000.00 del Val et al. (2014)
Cuba 6.20 166000.00 Padilla et al. (2020)

In this sense, the reported values are in the range from 1 to 7.6 g. In this case, the comparison is very difficult to carry out because it is necessary to know, if it was made based on full seeds (formed) or was quantified based on total seeds in the sample (full + empty), it is also important to specify the percentage purity of the sample or lot, to optimize the germination processes and guarantee the sowing and establishment of the species in this way.

The estimates of the number of seedlings per kg of seeds reported show a higher variability with minimum values of 17 000 seedlings determined in Colombia up to one million seedlings per kg of seed obtained in Mexico.

SEED GERMINATION

Although it is true that there are advances in the studies of the germination of this species, everything has not yet been resolved. Precisely, there is no coincidence if the T. diversifolia seeds have some kind of latency, since some authors (Agboola et al. 2006, Wen 2015 and Santo Gally et al. 2020) show that the seeds of this species have dormancy and others (Mattar et al. 2019 and Rodríguez et al. 2021) show that this species does not have latency.

Added to this is the lack of coincidence in relation to germination, since some researchers report that this species has low germination, reporting values between 25-35 % (Peters et al. 2002, Inayat, 2009, Angelovici et al. 2010 and Saavedra, 2016), however, there are other results that show that it is possible to exceed this seed quality indicator, reaching acceptable germinations between 60 and 90 % (Etejere and Oleyinka 2014) and Santo Gally et al. 2020).

In Cuba in the period 2017-2021 several researchers were developed where the germination percentage of different genetic materials collected in the central and western region of the country was evaluated. The germination capacity (table 2) ranged from 5 to 92 %, depending on the plant material. However, these same materials evaluated later showed percentages higher than 40 %, this variability may be related to the seed quality and the criteria that were used to define the best harvest time.

Table 2 Germination percentage of different T. diversifolia materials evaluated in Cuba 

Plant material Authors
3 5 10 13 16 17 23 24 25
19.00 19.00 4.00 89.00 49.00 92.00 19.00 22.00 89.00 Ruíz et al. (2018)
- - 43.70 - - - - - - Rodríguez et al. (2019)
58.25 - 54.75 - 53.25 - 52.00 - - Padilla et al. (2021)
- - 44.22 - - - 53.61 - 60.90 Rodríguez et al. (2021)

According to Etejere and Oleyinka (2014), the sowing depth is a factor that significantly affects the germination percentage. These authors determined in pots, germination at different depths (0, 0.5, 1.5, 2.5 and 3.5 cm) with respect to the soil surface, the highest germination percentage occurred at depth 0 cm (85 %), and decreased as depth increased. At depths from 0 to 2.5 cm the emergence occurred around 5 days, and at the depth of 3.5 cm the emergence started from the sixth day.

The differences in the germination percentages, both in laboratory researchers and in field sowings of gamic seed, may be due to the fact that the seeds were not collected at the best harvest time when the seeds were formed and have completed their maturation, because when this happens, seeds that are not completely formed are harvested, which induces a lower weight of 1000 seeds, germination percentage and production of pure germinable seed (PGS).

Akinola et al. (2000) in Nigeria studied six methods for breaking the dormancy of conserved seeds of T. diversifolia for 11 months (under environmental conditions). The methods of hot water at 80 and 100 ºC and dry air at 80 and 100 ºC, concentrated sulfuric acid (H2SO4) and 10 % hydrogen peroxide. These authors evaluated different exposure times to the treatments (0, 2.5, 5, 10, 15 and 20 minutes) and reached germination percentages higher than 65 % with the hot water treatment at 80 and 100 ºC (10 and 15 minutes) .

Recent studies by Padilla et al. (2021) when studying the effect of fixed and alternating temperatures and moistening with running water on the germination of Tithonia, showed that when the performance for a period of 30 days was evaluated (at intervals of 10 days) there were no differences between treatments. However, the high percentage of total germination of the seeds (76 and 84 %) is interesting, highlighting that in the first 10 days 67-75 % of them managed to germinate. In addition, less germination was required for the interval of 20-30 days, so it is not justified to extend the germination tests for more than 21 days.

Rodríguez et al. (2019) evaluated the germination percentage, under laboratory conditions, in Petri dishes and in bags in the nursery of Tithonia diversifolia (Hemsl.) material 10 where a total germination of 43.7 % was achieved in the bags and 54.9 % under laboratory conditions. The performance of some variables related to the morphostructure of the seedlings during the 45 days that their nursery stage lasted showed that Tithonia had a linear growth rate in height and number of leaves. This showed that the performance of this species under nursery conditions is adequate and allows obtaining vigorous seedlings ready for direct transplantation to the field with heights of 28.9 cm at 45 days after sowing. It is considered that it is at this time that the transplant to the field should be carried out since, due to the characteristics of flexibility that the stems of this species have, it is not advisable to wait any longer to avoid losses due to their fractionation.

Other results obtained in researches performed in Colombia show the efficiency of the use of nurseries to obtain seedlings, as long as the strictest protection measures for germinated seedlings are followed until transplantation (Solarte et al. 2013 and Summ 2015). Sanabria and Ávila (2015) determined seedling heights of 13.3 cm at 14 days after sowing and 69.7 cm at 60 days.

Many species require specific substrates to express their true germination potential. In this sense, Padilla et al. (2021) evaluated the germination percentage of Tithonia diversifolia material 16 using four substrates: Petri dishes using ground, cotton; cartons for transporting eggs using ground and in a moistened jute bag. The lowest germination percentage (7.75 %) occurred in the substrate of moistened jute bags. This negative result is important, since this practice is common in many farmers who carry out germination tests using this method and the germination power of the seed lot that is evaluated fundamentally in small seeds can be underestimated. In the rest of treatments, germination had a similar performance that ranged between 55-60 %. It was significant in this sense that when recycled cardboard containers with ground were used, good germination (60 %) was achieved, as was the case when Petri dishes with cotton and ground were used, which is the most widely used practice at the level of seed laboratories. This allows for several options to evaluate the germination percentage of this species.

Etejere and Olayinka (2015) also confirm the selectivity of this species, showing that the seedlings that emerged from the soil showed higher growth efficiency and vigor (81 %) compared to the seedlings obtained from seeds sown in Petri dishes (19 %).

The results reported in Cuba and other regions of the world in terms of the germination percentage show the possibility of using gamic seed for the propagation of this species, so the next step in the technological chain is the seed conservation.

SEED CONSERVATION

Research experiences carried out in Brazil (Mattar 2018) show seed conservation results based on two storage conditions (refrigerated and non-refrigerated environment) and two storage times (6 and 12 months). The refrigerated environment provided the highest percentages of seed germination, in addition, the speed of germination increased throughout the storage time. The seeds showed a high germination percentage after 12 months of storage, both under refrigerated and non-refrigerated conditions.

In this sense, Rodríguez et al. (2021) when evaluating three types of containers (plastic bottles with screw top, paper bags and nylon bags), and two storage conditions (cold room and environmental conditions), for the conservation of botanical seed of T. diversifolia material 10 began a study with seeds that had been harvested for 30 days and germinations higher than 60 %. The germination percentage of the seeds stored in the cold room ranged between 52.33 and 44.14 % for 60 and 540 days. A completely different performance, for the same period, was observed in those stored in the environment, that the seeds experienced a progressive drop in germination until reaching 12.67 % at 540 days. The differences between the two storage methods show the deterioration suffered by the seeds when stored at room temperature. After 365 days the seeds stored in the environment lost germination. Thus, for the 660 and 720 days after the start of storage, only the effect of the type of container with seeds that remained in the cold room was evaluated.

Tithonia seeds in the postharvest stage, previous to the beginning of storage, do not significantly deteriorate; while by increasing the storage time under uncontrolled conditions, they age at a progressive rate and lose germination after one year. Cold storage is recommended for the conservation of T. diversifolia seeds for long periods of time, as well as the use of the evaluated containers (plastic bottles, paper and nylon bags).

As can be seen, the analyzed results show the possibility of obtaining and using the gamic seed of this species for its propagation, as well as being satisfactorily preserved for periods of time of up to two years. However, guaranteeing the quality of seed alone does not allow reaching the levels of generalization and use of this species. The production of seed by gamic way needs to specify the yields of full seed and PGS ha-1 at the level of the primary farmer. This constituted a challenge for the scientific community and is what we propose to analyze below.

ADVANCES IN THE TECHNOLOGICAL PROCESS TO PRODUCE GAMIC SEED OF TREE MARIGOLD

In Colombia, various authors (Mahecha et al. 2015, Gallego-Castro, 2016 and Mahecha et al. 2017) made a first approach to the production of sexual seed of tree marigold where they characterized the number of stems and flowers, weight of fresh and dry flowers and number of seeds per plant and showed the possibility of a seed production from flower buds and calculated that 1 kg of seed contains 100 000 seeds. These novel results for that moment, showed the need to carry out new researchers at the field level that would facilitate the availability of a technology for the production of filled seed and PGS ha-1 and create the scientific bases for the production of commercial gamic seed.

The gamic seed production of this species is largely defined by the best harvest time. In general, the criteria used to determine the best harvest time for different species and varieties are the fixed dates after the appearance of anthesis, inflorescence color, moisture content, seed shelling, seed weight and fix the harvest time from the beginning of massive flowering (Padilla et al. 2018, Saavedra 2016, Suárez et al. 2018, Mattar et al. 2019, Santos-Gally et al. 2019, Padilla et al. 2020 and Santos- Gally et al. 2020).

However, regardless of the method used in each research, the practical recommendation must be accompanied by phenological and morphological changes, as well as quantitative and qualitative information that allow defining in the field the precise moment that the harvest should be carried out by the technicians and primary farmers.

At the Institute of Animal Science from Cuba Padilla et al. (2018) showed for the first time in the three phenological stages of inflorescence development that there is the presence of formed seeds able to germinating (seed heads with green bracts and withered petals, seed heads with green bracts without petals and seed heads with bracts and dry brown peduncles).

It was pointed out that when it is harvested in the state of green bracts without petals, there is the lowest weight of full seeds and the highest weight of empty per seed heads. With this, it was defined that in this phenological state of the seed heads, the empty seeds have not yet shelled and the full ones have not completed their formation and physiological maturation. On the other hand, the germination percentage was higher (48.25 %) when the seed heads were harvested with bracts and dry brown peduncles compared to those harvested with green bracts and without petals (34.50 %), however, the production of filled seed was inverse (192 and 156 mg. seed head-1, respectively). Hence, to specify the best harvest time, the production of PGS. seed head -1 must be taken into account, which was similar in both treatments, this is the most transcendental indicator for the technological output of gamic seed production of tree marigold.

On the other hand, when analyzing the weight of 1000 seeds, it was observed that when the seed heads are harvested in the phenological state of green bracts and withered petals, there is still no complete formation of the seed, which allows concluding that the best time of seed harvest is achieved when the panicles are harvested in the state of green seed heads without petals and seed heads with bracts and dry brown peduncles where there is a greater formation and maturation of the seeds, this is the period where the production of full seeds and the germination percentage was compensated.

The previous results allowed advancing in other studies (Padilla et al. 2021) to define the best harvest time that included a greater range of characterization of harvest times according to the phenological and morphological changes that occur in seed heads in the time and evaluating the yields of filled seed and PGS.

Photo 1 and 2 show the phenological changes that occur in the seed heads during the process of maturation and formation of achenes and the phenological stages that produce seeds are defined according to the morphology of the seed heads, as well as color changes that occur from the beginning of massive flowering. This moment occurs when of the total number of stems with inflorescences in the field, half have flowers and buds, while the other half are in the seed phase (seed heads with green bracts and withered petals, seed heads with green bracts and yellow corollas, seed heads with green bracts and brown corollas and seed heads with dry bracts and peduncles, colored brown).

Photo 1 Inflorescences that do not produce seeds. A- Closed bud, B- Open bud, C- Flower 

Photo 2 Inflorescences that produce seeds. D- Seed heads with green bracts and withered petals, E- Seed heads with green bracts and yellows corollas, F- Seed heads with green bracts and brown corollas, G- Seed heads with dry bracts and peduncles (brown) 

The results show that the harvest should be carried out when in the field between 80-93 % of the total inflorescences that produce seeds predominate and the presence of seed heads with dry bracts and peduncles colored brown ranges between 20-60 %, this can be achieved between the 12 and 20 days after the massive flowering started (figure 1).

Figure 1 Performance of seed production during the harvest period 

This performance is supported by the fact that at this precise moment is when the highest weights of full seeds of the stems with flowers and full seeds heads-1 are achieved. This criterion is also validated by the weight of the germinated seedlings and the weight of 1000 seeds, which were also the indicators with the best performance for that same harvest time and confirms the need for the seeds to complete their formation and physiological maturation before being harvested. These results are novel, because for the first time it is possible to define quantitatively and qualitatively the best harvest time for the tree marigold at the field level, where yields of the order of 33 kgha-1 of filled seeds and 24 kg of PGS ha-1 were achieved when the harvest is carried out between 12 and 20 days after the massive flowering begins. These yields are considered good, if it is taken into account that one kilogram of seed contains around 166,000 full seeds according to the Tithonia plant materials studied (Padilla et al. 2020).

After defining the best harvest time, Padilla et al. (2021) evaluated three cut moments (May-July-September) in four outstanding materials (3, 10, 16 and 23) for a period of three years. The results of this research allowed defining the preponderant role of the moment of application of predetermined cuts to promote massive flow of flowering in the fertile stems of this species. With this, a greater uniformity of the phenological development of the seed heads was guaranteed over time, affecting the formation and more uniform maturation of the seeds that facilitates the definition and precision of the best harvest time.

The agronomic management with the use of different moments of applying cuts, allowed to define, in the first place, that the four materials used did not have a uniform response, thus material 16 was the only one that managed to produce seed from the second year of study when the cut was applied in July, the other evaluated materials did not achieve it. Furthermore, when cutting in September none of the plant materials produced seed from the second year. This defined the plant’s need for a period of 4-6 months to achieve the formation of fertile stems and the development and formation of seeds, which constitutes a novel scientific result for the species. This period coincides with the beginning of the rainy period, after stabilizing the rainfalls in Cuba, where the climatic conditions of daylight and temperature occur that favor massive flowering and the formation and physiological development of the seed with acceptable germination percentages and higher yields of pure germinable seed.

Independent of the interactions that occurred between the time of applying the cut and the materials studied for the first year; when the four materials were fully evaluated, the 16th highlighted for the highest yields of full seeds, PGS, and weight of 1000 seeds, mainly when cutting was applied in July to cause massive and uniform flows of fertile stems.

The gamic seed production reached by material 16 in this study is of the order of 49.45 -98.89 kg.ha-1 of full seed and 26.63- 53.26 kg.ha-1 PGS for the second and third year. This excellent yield was greatly favored because the harvest was carried out at the optimum time according to Padilla et al. (2020) and this confirms the hypothesis that the production of gamic seed of Tithonia diversifolia is possible. In addition, it contributes to the scientific knowledge that there are marked differences in the production of seeds between the studied plant materials. The previous supports the genetic differences of these materials that were reported by Ruíz et al. (2018) in the biomass production for its use in cutting and grazing.

Although it is true that material 16 highlighted, also materials 3, 10 and 23 reached acceptable PGS yields, taking into account that a kg of full seeds can have around 166 600 seeds with more than 95 % purity and germination percentages between 50-80 %, it should then be considered that these materials should also be used in the production programs of gamic seeds of this species.

SOWING AND ESTABLISHMENT BY GAMIC SEED

As mentioned above, until the 2010-2017 period there was no information available showing the possibility of sowing this species directly in the gamic seed field. In this sense, there is a deficiency in literary records on the propagation through this way.

The propagation of this plant is done almost 100 % through the use of cuttings, which are easy to acquire from other crops. Several are the researchers related to the plantation of the tree marigold by agamic seed (Almeida et al. 2009, González et al. 2013, Zapata and Vargas 2014, Lourenco et al. 2015 and Gallego-Castro et al. 2017) where it is define different aspects such as: stem section, planting form and even the application of synthetic auxins to stimulate rooting was evaluated (dos Santos Silva et al. 2018). However, it should be highlighted that this type of propagation have some difficulties such as transport and storage that can only be carried out during short periods, without affecting the quality of cuttings (Sánchez et al. 2014), in addition to the increase in planting costs .

The experience in Colombia of gamic seed sowings of tree marigold is showed in several researchers such as: Mahecha et al. (2015), Gallego- Castro (2016) and Mahecha et al. (2017), but in these cases the seedlings obtained in germinators are carefully selected, either to transplant them into nursery bags or to sow them directly in well-prepared soils.

Other more recent experiences in Mexico (Cortez et al. 2019 and Uu-Espens et al. 2019) also use seedling transplantation, as did Gallego-Castro et al. (2015) in Colombia.

The first experiences in Cuba (Padilla et al. 2021) when evaluating under field conditions the establishment of T. diversifolia sowing by gamic seed and transplanting in bags compared to the traditional method of planting by cuttings, showed that two years after the sowing, the population of stems and tillers.m2, leaves, stems and the percentage of leaves, as well as the height and stem diameter were similar in all treatments. There were also not significant differences for the yield, which was of the order of 3.64- 4.42 tDM ha-1 cut-1 at 90 days.

In other experiments still under development, where the same quantity of seeds and buds of the stems per plots was guaranteed, the possibilities of sowing by gamic seed are more evident in relation to agamic plantations and transplantation in bags. Thus, under field conditions, at 7 days, the sowing by seed had achieved to germinate with a population of 2.63 plants m-2 while the plantations by cuttings had not yet started germination and at 41 days it reached 3.76 plants m-2, a higher value to the planting by stems that only reached 2.60 plants m-2.

The results in the first establishment cut at180 days reaffirm the superiority of the sowing by gamic seed in relation with the plantations by cuttings. Thus, the highest yield (11.68 tDM.ha-1) was achieved in the sowing with by gamic seed that differs from the plantations by stem (9.92 tDM.ha-1) and in bags (9.48 tDM.ha-1).So, the populations in the sowing by gamic seed direct to the soil or transplanted in bag (10.55 and 10.88 stems.m2, respectively) were higher to the ones planted by cuttings (5.80 stems.m-2).

In other researchers Padilla et al. (2020a) achieved progress on the real possibility of obtaining satisfactory establishments when different protection practices of gamic seed of T. diversifolia material 16 were used in a Eutric Red Ferralitic soil. The results showed that, in the population performance, in the samplings carried out at 30 and 60 days after sowing, it could seen a lower population in the control (3 plants m-2) without covering and there were not differences between the use of organic matter or plant wastes with a population of 8 and 13 plants m-2, respectively.

The stage of development of the seedlings at 60 days after sowing was favored by covering the seeds with organic matter (OM) where the height, stem diameter and number of leaves stem-1 had a better performance for this early stage of Tithonia establishment by gamic seed. The yields of 4.00 tDM.ha-1.cut-1 achieved in direct sowings in the field by gamic seed during the establishment phase of Tithonia, are acceptable and novel, since no previous reports of biomass production are known, when this way of propagation is used.

Although it is true that applying covering with cattle manure in the early stages of plant development was advantageous for some components of the yield from the first and second cut, it was found that at the end of the study the results are similar for all the evaluated treatments. That is why both treatments should be recommended as coverings (Mulch) to improve germination, survival of young seedlings and biomass production of different T. diversifolia materials when sowing under field conditions with botanical seeds are carried out. On the other hand, putting both options in the hands of the primary farmers is practical, since it gives the possibility of choosing the one that is most feasible according to availability and cost at the regional level.

When evaluating different levels of coverings (0, 250, 338 and 500 g.m-2) with vegetable stubble, in the germination, survival and establishment by gamic seed of T. diversifolia cv material 10 under field conditions, Padilla et al. (2021) showed that the germination percentage was lower at 12 and 30 days after sowing in the control, which was similar to the treatment of 250 g.m-2 of coverings. In general, there was a linear increase in the germination percentage in the field with the increase in the coverings levels. The fact that with the use of the highest level of coverings (500 gm-2), the seeds achieve 28.8 % germination at 12 days and 29.84 % at 30 days with the medium level (338 g m-2) after sowing, endorses the benefits of this practice for the establishment of Tithonia. The fact that the seeds sown in the field in just 12 days managed to germinate 58% with respect to their potential in the laboratory, is a good indicator that enhances the hypothesis of establishing the tree marigold by gamic seed. The previous results are strengthened with the biomass yields reached in the first establishment cut 120 days after sowing of the order of 6 -11 tDM.ha-1.cut -1 and in the second and third cuts made at 90 days, yields of 2.02 tDM.ha-1.cut -1 were obtained in the dry season and up to 6.00 tDM ha-1 .cut-1 when it coincided with the rainy season for the best results with the application of coverings levels of plant wastes between 338-500 g.m-2 (Padilla et al. 2021).

In the three cuts made in the establishment phase, the performance of the indicators: population, height, stem diameter and number of leaves and tillers.plant-1 also showed the beneficial effect of the coverings application, lasting the improvements produced in the early stages of development before undergoing the cut. These results reaffirm the benefits of using vegetable coverings in the establishment of this plant reported by Padilla et al. (2020a) in soil and climate conditions similar to that of the study, when the seeds are sown directly into the soil under field conditions.

Establishing a technique of direct sowing of gamic seed in the field constitutes a task of the first order, which would allow the successful establishment of this species. These results make it possible to eliminate the nursery and transplant phase, which constitutes a difficult process, especially when the technological result is aimed at medium and large scale for the sowing and establishment of tree marigold.

GENERAL CONSIDERATIONS

Due to its productive response and persistence in livestock systems as forage or grazing plant, today Tithonia diversifolia constitutes the preferred species by farmers in Cuba within the protein plants group. However, its accelerated implementation has been limited by not having a technology for the production of seed and establishment by gamic way and eliminating the difficulties that its vegetative propagation by cuttings represents. The results obtained in Cuba provide a technology that integrates the production of seed and the establishment by gamic way, which constitutes a novel scientific contribution that will make possible a greater production and commercialization of seed.

The alternative of propagation by gamic way puts in the hands of farmers, technicians and managers a more feasible biological, practical and economic option for the propagation of this species.

Facing the challenge of accelerating the production of seed and its establishment through the gamic way constitutes today an urgent need for the implantation of forage production systems and its use in grazing. There is also no doubt by scientists, farmers and managers that this is the best option for the accelerated propagation of the species for the medium and large productive scale due to the biological, practical and economic limitations that vegetative plantations imply, which is the method currently used.

To guarantee the introduction of these results, it is recommend training and advising farmers, technicians and managers in the achieved technology and ensuring that the equipment and implements for harvesting and post-harvesting of seeds are guaranteed by specialized enterprises.

REFERENCES

Agboola, D.A, Idowu, W.F. & Kadiri, M. 2006. "Seed germination and seedling growth of the Mexican sunflower Tithonia diversifolia (Compositae) in Nigeria, África". Revista de Biología Tropical, 54(2): 395-402, ISSN: 0034-7744. [ Links ]

Akinola, J.O., Larbi, A., Farinu, G.O & Odunsi, A.A. 2000. "Seed treatment methods and duration effects on germination of wild sunflower". Experimental Agriculture, 36(1): 63-69, ISSN: 1469-4441. https://doi.org/10.1017/S0014479700361075. [ Links ]

Alcorcés, N., Lárez, A & Mayz, J. 2007. "Adiciones al conocimiento citogenético de Tithonia diversifolia (hemsl.) A. gray (Asteraceae) ". Acta Botánica Venezuelica, 30(2): 267-275, ISSN: 0084-5906. [ Links ]

Almeida, A.P., da Silva Xavier, A y de Arruda, L. A. M. 2009. "Influência do tipo de estaca na propagação de Tithonia diversifolia (Hemsley) Gray". Environmental Research, 3: 39-46, ISSN: 1096-0953. [ Links ]

Angelovici, R., Galili, G., Fernie, A.R & Fait, A. 2010. "Seed desiccation: a bridge between maturation and germination". Trends in Plant Science, 15(4): 211-218, ISSN: 1878-4372. https://doi.org/10.1016/j.tplants.2010.01.003. [ Links ]

Cortez, D.E.C., Blandon, O.J.O & Vélez, S.A.T. 2019. "Experiencias en campo a partir de la reproducción sexual de botón de oro Thitonia diversifolia-semillero de investigación sipass". Revista Agricolae & Habitat, 2(1), ISSN: 2665-3176. https://doi.org/10.22490/26653176.3522. [ Links ]

Del Val, R., Miranda, J.M., Xochitl, M., Solorio, B., Solorio, F.J., Gómez, J.F. & González, S. 2014. "Diversidad genética de Tithonia diversifolia (Hemsl) gray de Michoacán: análisis con marcadores de ADN-SSR". Ciencia y tecnología universitaria, 4(3), ISSN: 2007-7750. [ Links ]

dos Santos Silva, A. M., da Silvam, L, D., Santos, M. V., da Cruz, P. J. R & Titon, M. 2018. "Propagação vegetativa de Tithonia diversifolia com ácido indolbutírico. Livestock Research for Rural Development, 30(5), Article #90, ISSN: 0121-3784, Available: http://www.lrrd.org/lrrd30/5/alex30090.html. [ Links ]

Durant, N., Lenin, J., Ruíz, J.A., González, D., García, J., Martínez, S & Crespo, M. 2020. "Impacto del cambio climático en la distribución potencial de Tithonia diversifolia (Hemsl.) A. Gray en México". Revista Mexicana de Ciencias Pecuarias, 11: 93-106, ISSN: 2448-6698. https://doi.org/10.22319/rmcp.v11s2.4705. [ Links ]

Etejere, E. & Olayinka, U. 2014. "Seed production, germination, emergence and growth of Tithonia diversifolia (HEMSL) A. Gray as influenced by different sowing depths and soil types". American-Eurasian Journal of Agricultural and Environmental Sciences, 14(5): 440-444, ISSN: 1990-4053. https://doi.org/10.5829/idosi.aejaes.2014.14.05.12331. [ Links ]

Etejere, E.O & Olayinka, B. U. 2015. "Seed Production, Germination, Emergence and Growth of Tithonia diversifolia (Hemsl.) A. Gray as Influenced by Different Sowing Depths and Soil Types". Albanian Journal Agricultural Sciences, 14(3): 294-299, ISSN: 2218-2020. [ Links ]

Galindo, A., Romero, O.M., Murgueitio, E. & Calle, Z. 2011. "El botón de oro: Un caso innovador sobre cómo propagarlo". Revista Carta FEDEGAN, 126: 72-75, ISSN: 0123-2312. [ Links ]

Gallego-Castro, L.A. 2016. Evaluación agronómica y análisis productivo del botón de oro como suplemento alimenticio de vacas lecheras en trópico alto. MSc. Thesis. Universidad de Antioquia, Antioquia, Colombia. [ Links ]

Gallego-Castro, L.A., Ledesma, L. M y Arizala, J. A. 2015. Crecimiento y desarrollo de Tithonia diversifolia Hemsl. A Gray en condiciones de trópico alto. Memorias 3° Congreso Nacional de Sistemas Silvopastoriles-VIII Congreso Internacional de Sistemas Agroforestales, Ciudad Autónoma de Buenos Aires, Argentina. [ Links ]

Gallego-Castro, L.A., Mahecha-Ledesma, L & Angulo-Arizala, J. 2017. "Calidad nutricional de Tithonia diversifolia Hemsl. A Gray bajo tres sistemas de siembra en el trópico alto". Agronomía Mesoamericana, 28(1): 213-222, ISSN: 2215-3608. [ Links ]

González, D., Ruíz, T.E & Díaz, H. 2013. "Stem section and planting method: its effect on Tithonia diversifolia biomass production". Cuban Journal of Agricultural Science, 47(4): 425-429, ISSN: 2079-3480. [ Links ]

González-Castillo, J.C., Hahn Von-Hessberg, C.M y Narváez-Solarte, W. 2014. "Características botánicas de Tithonia diversifolia (Asterales: Asteraceae) y su uso en la alimentación animal". Boletín Científico Centro de Museos de Historia Natural de la Universidad de Caldas, 18(2): 45-58, ISSN: 0123-3068. [ Links ]

Guerra, N., Lárez, A & Mayz, J. 2007. "Adiciones al conocimiento citogenético de Tithonia diversifolia (HEMSL.) A. Gray (Asteraceae) ". Acta Botánica Venezuelica, 30(2): 267-275, ISSN: 0084-5906. [ Links ]

Holguín, V.A., Ortiz, S., Velasco, A. & Mora-Delgado, J. 2015. "Evaluación multicriterio de 44 introducciones de Tithonia diversifolia (Hemsl.) A. Gray en Candelaria, Valle del Cauca". Revista de la Facultad de Medicina Veterinaria y de Zootecnia, 62(2): 57-72, ISSN: 2357-3813. https://doi.org/10.15446/rfmvz.v62n2.51995. [ Links ]

Inayat, A. 2009. Influencia de las fases lunares (Menguante y Luna llena) sobre la propagación vegetativa del botón de oro Tithonia diversifolia para la formación de un banco de proteína. Diploma Thesis. Facultad de Ingeniería de Ciencias Agropecuarias, Escuela Politécnica del Ejército, El Prado, Quito, Ecuador. [ Links ]

Jing, Y., Ling, T., Ya-Li, G & Wei-Bang, S. 2012. "Genetic Diversity of an Alien Invasive Plant Mexican Sunflower (Tithonia diversifolia) in China". Weed Science, 60(4): 552-557, ISSN: 1550-2759. https://doi.org/10.1614/WS-D-11-00175.1. [ Links ]

La Duke, J.C. 1980. Systematics of Tithonia desf. Ex gmelin (COMPOSITAE, HELIANTHEAE). PhD Thesis. Graduate School of the Ohio State University, USA, p. 187. [ Links ]

Lourenco, J.D.P., Matos, A.D.O., de Meirelle, A.C & da Silva, R.L. & Lourenco, F. S. 2015. Estudos preliminares sobre a propagação vegetativa de Tithonia diversifolia. In: Embrapa Amazônia Ocidental-Artigo em Anais de Congresso (ALICE). Congresso Brasileiro De Agroecologia. Belém, Pará, Brasil. [ Links ]

Mahecha, L., Angulo, J. & Barragán, W. 2015. Efecto de la sombra en cambios estructurales de Brachiarias asociadas a T. diversifolia y/o C. argentea. In: Memorias 3° Congreso Nacional de Sistemas Silvopastoriles / compilado por Pablo L. Peri. 1st Ed. Ed. INTA. Santa Cruz, Argentina, p.294, ISBN: 978-987-521-611-2. [ Links ]

Mahecha-Ledesma, L., Angulo-Arizala, J. & Barragán-Hernández, W. 2017. "Calidad nutricional, dinámica fermentativa y producción de metano de arreglos silvopastoriles". Agrononomía Mesoamericana, 28(2): 371-387, ISSN: 2215-3608. https://doi.org/10.15517/MA.V28I2.22750. [ Links ]

Mattar, E. 2018. Propagação e conservação de espécies arbustivas de uso múltiplo: Tithonia diversifolia e Cratylia argentea. PhD Thesis. Universidade Federal de Viçosa, Vicosa, Brasil. [ Links ]

Mattar, E., Vianna, T.T., Pereira, W.D., Brasileiro, B.P., Hilst, P.C. & Días, D.F. 2019. "Physiological quality of Tithonia diversifolia (Hemsl.) A. Gray seeds as a function of harvest period and storage conditions". Bulgarian Journal of Agricultural Science, 25(6): 1133-1142. ISSN: 1310-0351. [ Links ]

Muoghalu, J.I. 2008. "Growth, reproduction and resource allocation of Tithonia diversifolia and Tithonia rotundifolia". Weed Research, 48(2): 157-162, ISSN: 1365-3180. https://doi.org/10.1111/j.1365-3180.2007.00613.x. [ Links ]

Muoghalu, J.I. & Chuba, D.K. 2005. "Seed germination and reproductive strategies Tithonia species". Applied Ecology and Environmental Research, 3(1): 39-46, ISSN: 1589-1623. [ Links ]

Obiakara, M. & Forcade, Y. 2018. "Climatic niche and potential distribution of Tithonia diversifolia (Hemsl.) A. Gray in Africa. Africa". PLoS ONE, 13(9): e0202421, ISSN: 1932-6203. https://doi.org/10.1371/journal.pone.0202421. [ Links ]

Padilla, C., Rodríguez, I., Ruíz, T.E., Herrera, M. 2018. "Determinación del mejor momento de cosecha de semilla gámica, Tithonia diversifolia (Hemsl.) Gray". Livestock Research for Rural Development, 30(4), Article #71, ISSN: 0121-3784, Available: http://www.lrrd.org/lrrd30/4/idal30071.html. [ Links ]

Padilla, C., Rodríguez, I., Ruíz, T.E., Herrera, M. 2021. Evaluación del establecimiento y producción de biomasa a partir de la semilla gámica y agámica de Tithonia diversifolia. In: Informe Final de Proyecto: Diversificación, mejoramiento y multiplicación de recursos fitogenéticos de especies productoras de forrajes de alta calidad para la alimentación animal. Departamento de Pastos y Forrajes, Instituto de Ciencia Animal, Mayabeque, Cuba, pp. 304-307. [ Links ]

Padilla, C., Rodríguez, I., Ruíz, T.E., Herrera, M., Mesa, Y., Sarduy, L. & Díaz, L. 2020a. "Mejor momento de cosecha en producción y calidad de semilla gámica de Tithonia según estado fenológico de la estructura floral". Livestock Research for Rural Development 32(3), Article #146, ISSN: 0121-3784, Available: https://www.lrrd.cipav.org.co/lrrd32/9/idalm32146.htm.lLinks ]

Padilla, C., Rodríguez, I., Ruíz, T.E., Ojeda, M., Sarduy, L. & Díaz, L. 2020b. "Evaluación de diferentes prácticas de protección de la semilla gámica en el establecimiento de Tithonia diversifolia (Hemsl.) Gray vc material 16". Livestock Research for Rural Development, 32(3), Article #50, ISSN: 0121-3784, Available: https://lrrd.cipav.org.co/lrrd32/3/idal32050.html. [ Links ]

Paniagua-Hernández, L.D., Arias-Gamboa, L.M., Alpízar-Naranjo, A., Castillo-Umaña, M.Á., Camacho-Cascante, M.I., Padilla-Fallas, J.E. & Campos-Aguilar, M. 2020. "Efecto de la densidad de siembra y edad de rebrote en la producción y composición bromatológica de Tithonia diversifolia (Hemsl.) A. Gray". Pastos y Forrajes, 43(4): 275-283, ISSN: 2078-8452. [ Links ]

Pérez, A., Montejo, I., Iglesias, J., López, O., Martín, G., García, D., Idolkis, M & Hernández, A. 2009. "Tithonia diversifolia (Hemsl.) A. Gray". Pastos y Forrajes, 32(1): 1-15, ISSN: 2078-8452. [ Links ]

Peters, M., Franco, I.H., Schmidt, A. & Hincapié, B. 2002. Especies forrajeras multipropósito: opciones para productores de Centroamérica. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia. [ Links ]

Rivera, J.H. 2020. Variabilidad fenotípica y genética de Tithonia diversifolia (hemsl.) A. Gray, una planta para la producción animal sostenible en Colombia. PhD Thesis. Medellín, Antioquia, Colombia. [ Links ]

Rodríguez, I., Padilla, C & Medina, Y. 2021. Características de la estructura floral y evaluación de la producción de semillas de diferentes materiales de Tithonia diversifolia Hemsl.) A. Gray. en Cuba. In: Informe Final de Proyecto: Diversificación, mejoramiento y multiplicación de recursos fitogenéticos de especies productoras de forrajes de alta calidad para la alimentación animal. Departamento de Pastos y Forrajes, Instituto de Ciencia Animal, Mayabeque, Cuba, pp. 304-307. [ Links ]

Rodríguez, I., Padilla, C. & Ojeda, M. 2019. "Características de la germinación de la semilla gámica de Tithonia diversifolia (Hemsl.) Gray y su comportamiento en condiciones de vivero". Livestock Research for Rural Development, 31(5), Article #69 , ISSN: 0121-3784, Available: http://www.lrrd.org/lrrd31/5/idalma31069.html. [ Links ]

Romero, O., Galindo, A., Murgueitio, E. & Calle, Z. 2014. "Primeras experiencias en la propagación del botón de oro (Tithonia diversifolia, Hemsl. Gray) a partir de semillas para la siembra de sistemas silvopastoriles intensivos en Colombia". Tropical and Subtropical Agroecosystems, 17(3): 525-528, ISSN: 1870-0462. [ Links ]

Ruíz, T.E., Alonso, J., Febles, G.J., Galindo, J.L., Savon, L.L., Chongo, B., Martínez, Y., La O, O., Cino, D.M., Crespo, G.J., Mora, L., Valenciaga, N., Padilla, C., Rodríguez, B., Muir, L., Rivero, A., Hernández, N. 2017. Evaluación de materiales recolectados de Tithonia diversifolia (Hemsl) Gray en Cuba. Chará, J., Peri, P. y Rivera J., (eds). Actas IX Congreso Sistemas Silvopastoriles. Aporte a los objetivos de desarrollo sostenible. Cali, Colombia, p. 486. [ Links ]

Ruíz, T.E., Febles, G., Achan, G., Díaz, H. & González, J. 2018. "Capacidad germinativa de semilla gámica de materiales colectados de Tithonia diversifolia (Hemsl.) Gray en la zona centro-occidental de Cuba". Livestock Research for Rural Development, 30(5), Article #81, ISSN: 0121-3784, Available: http://www.lrrd.org/lrrd30/5/ruiz30081.html. [ Links ]

Saavedra, S. 2016. Fenología y fisiología de semillas de botón de oro Tithonia diversifolia (Hemsl.) Gray. MSc. Thesis. Facultad de Ciencias Agrarias, Universidad Nacional de Colombia, Medellín, Colombia. [ Links ]

Sanabria, E. & Ávila, I. 2015. Producción de follaje de la especie botón de oro (Tithonia diversifolia) utilizando 5 técnicas de siembra con fines de alimentación animal. Diploma Thesis. Universidad Nacional Abierta y a Distancia UNAD, Colombia. [ Links ]

Sánchez, L. Marcela., Hernández, Marcela & Sánchez, H. 2014. "Dynamics agro technique and germination for efficient development of Tithonia diversifolia". Sistemas de Producción Agroecológica, 5(2): 59-81, ISSN: 2248-4817. [ Links ]

Santos-Gally, R., Boege, K., Fornoni, F. & Domínguez, C. 2017. Ganadería sostenible en la región de Los Tuxtlas, Veracruz, México: el equilibrio entre la producción y la conservación de la biodiversidad. Chará, J., Peri, P. & Rivera, J., (eds). Actas IX Congreso Sistemas Silvopastoriles. Aporte a los objetivos de desarrollo sostenible. Cali, Colombia, p. 318. [ Links ]

Santos-Gally, R., Muñoz, M. & Franco, G. 2019. Efecto de la latencia sobre la germinación de Tithonia diversifolia (Asteraceae). X Congreso Internacional de sistemas silvopastoriles por una producción sostenible. Libro de Actas. Rivera, J., Peri, P., Char, J., Díaz, M., Colcombet, L. & Murgueitio, E. (eds). Ed. CIPAV, ISBN: 978-958-9386-91-0, p. 420. [ Links ]

Santos-Gally, R., Muñoz, M. & Franco, G. 2020. "Fruit heteromorphism and germination success in the perennial shrub Tithonia diversifolia (Asteraceae) ". Flora, 271: 151686, ISSN: 0367-2530. https://doi.org/10.1016/j.flora.2020.151686. [ Links ]

Silva, N.P.C., da Veiga, M. de J.V. & Machado, V.L.L. 1990. "Visiting insects of Tithonia diversifolia (Hemsl.) A. Gray (Compositae) during their flowering period". Bioikos, 12(1/2): 19-28, ISSN: 0102-9568. [ Links ]

Solarte, L.H., Murgueitio, E., González, J.G., Uribe, F. & Manzano, L. 2013. Protocolo para la siembra de botón de oro y leucaena en potreros con praderas mejoradas para el establecimiento de sistemas silvopastoriles intensivos. Fundación CIPAV, Bogotá, Colombia. [ Links ]

Suárez, J., Ayala, K. & Gómez, J.C. 2018. Sistemas Silvopastoriles Intensivos SSPi. In: Proyecto Ganadería Colombiana Sostenible. Available: www.ganaderiacolombianasostenible.co. [ Links ]

Summ, D. 2015. Como cultivar el botón de oro (Tithonia diversifolia) en Colombia. Available: http://www.monografias.com/trabajos101/como-cultivar-boton-oro-colombia/como-cultivar-boton-oro-colombia.html, [Consulted: May 15, 2015]. [ Links ]

Tiebre, M.S., Kassi, N.J., Kouadio, Y.J. & N’Guessan, E.K. 2012. "Etude de la biologie reproductive de Tithonia diversifolia (Hemsl.) Gray (Asteraceae): Espèce non indigène invasive en Côte d’Ivoire". Journal of Asian Scientific Research, 2(4): 200-211, ISSN: 2226-5724. [ Links ]

Uu-Espens, C.E.A., Escobedo-Cabrera, A., Cabañas-Gallardo, A.J., Chay-Canul, V., Díaz- Echeverría, F., Casanova-Lugo, F. & Piñeiro-Vázquez, A.T. 2019. "Establecimiento de un banco de forraje de Tithonia diversifolia en el sur de Quintana Roo, México". Revista Mexicana de Agroecosistemas, 6: 1289-1294, ISSN: 2007-9559. [ Links ]

Wang, S-H., Sun, W. & Cheng, X. 2004. "Attributes of plant proliferation, geografic spred and the natural communities invaded by naturalized alien plant species Tithonia diversifolia in Yunnan, China". Acta Ecologica Sinica, 24(3): 444-449, ISSN: 1872-2032. [ Links ]

Wang, S.H., Sun, W.B., Cheng, X. & Yang, Y.M. 2008. "Reproductive characteristics of Tithonia diversifolia and its geographical spread in Yunnan Province of South-West China". Acta Ecologica Sinica, 28(3): 1307-1313, ISSN: 1872-2032. [ Links ]

Wen, B. 2015. "Effects of High Temperature and Water Stress on Seed Germination of the Invasive Species Mexican Sunflower". PLoS ONE, 10(10): e0141567, ISSN: 1932-6203. https://doi.org/10.1371/journal.pone.0141567. [ Links ]

Zapata, A. & Vargas, J.E. 2014. Botón de oro: Manual para su establecimiento y manejo en sistemas ganaderos. 1st Ed. Ed. Universidad de Caldas, Manizales, Caldas, Colombia. [ Links ]

Received: June 27, 2021; Accepted: August 01, 2021

*Email:cpadilla@ica.co.cu

Conflict of interest: The authors declare that there are no conflicts of interests among them

Author´s contribution: César Padilla Corrales: Original idea, data analysis, writing the manuscript. Idalmis Rodríguez García: Data analysis, writing the manuscript

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