Germination rate and cardinal temperatures in Chenopodium quinoa Suyana and Tunkahuan varieties

D. Ramírez-Santiago1; G. H. De-La-Cruz-Guzmán1*; E. Espitia-Rangel2; S. Sampayo-Maldonado1; M. Mandujano-Piña1; A. Arriaga-Frías1

1. Unidad de Morfología y Función, Facultad de Estudios Superiores Iztacala, UNAM. Av. de los Barrios Núm. 1, Los Reyes Iztacala, Tlalnepantla, Estado de México. México. C. P. 54090., Universidad Nacional Autónoma de México, Unidad de Morfología y Función, Facultad de Estudios Superiores Iztacala, UNAM,

<city>Tlalnepantla</city>
<state>Estado de México. México</state>
<postal-code>54090</postal-code>
, Mexico , 2. Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias (INIFAP). Av. Progreso 5, Santa Catarina, Ciudad de México, CDMX, México. C. P. 04010., Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias,
<state>CDMX</state>
<postal-code>04010</postal-code>
, Mexico

Correspondence: *. Corresponding Author: Gumercindo Honorato, De-La-Cruz-Guzmán. Unidad de Morfología y Función, Facultad de Estudios Superiores Iztacala, UNAM. Av. de los Barrios Núm. 1, Los Reyes Iztacala, Tlalnepantla, Estado de México. México. C. P. 54090. Phone: +52 555 623 1257. E-mail: E-mail: ., http://www.iztacala.unam.mx


ABSTRACT

The effect of ten temperatures (5, 10, 15, 20, 25, 30, 35, 40, 45 and 50 °C) on germination of Chenopodium quinoa Suyana and Tunkahuan was evaluated. The seeds of each variety were harvested during the spring-summer 2017 cycle in Texcoco, state of Mexico and donated for this research in February 2019. The experimental units were 100 x 15 mm Petri dishes, with two double discs of absorbent paper moistened with 5 mL of distilled water, and 100 seeds of Suyana or Tunkahuan. The treatments with five replicates were each one of the temperatures. For germination, five experimental units of each variety were placed into incubators under total darkness, adjusted to the mentioned temperatures ± 0.5 °C. The following parameters were evaluated: total germination, germination rate, average germination (t50) and cardinal temperatures. In the Tunkahuan variety, germination higher than 90 % occurred between 5 and 40 °C, whereas in Suyana it occurred between 15 and 35 °C. Germination rate was higher in Suyana than in Tunkahuan and it occurred between 30 and 40 °C. The t50 value was obtained in less time in Tunkahuan (7.1 h) than in Suyana (8.1 h). Basal, optimum and maximum temperatures were: 2.3 and 1.8; 30.2 and 33.2; 48.8 and 62.2 °C for Suyana and Tunkahuan, respectively. In conclusion, Tunkahuan seeds germinated successfully in a wider range of temperatures, which could improve their establishment in arid and warm areas.

Received: 2019 November 24; Accepted: 2020 June 22

revbio. 2020 Aug 7; 7: e880
doi: 10.15741/revbio.07.e880

Keywords: KEY WORDS: Total germination, average germination, basal temperature, optimum temperature, maximum temperature, quinoa.

Introduction

Quinoa (Chenopodium quinoa Willd) is a species of the Amaranthaceae family, having a high potential of cultivation due to its nutritional properties, adaptation to diverse habitats and genetic diversity (Abugoch-James, 2009; Bhargava and Srivastava, 2013). The prehispanic civilizations of Peru and Bolivia located in the surroundings of Titicaca lake began its domestication in 8000 or 7500 BC (Zurita-Silvia et al., 2014).

In the Andean region, quinoa is widely cultivated and has been classified into five ecotypes according to the sites where it is grown: From valley, which grows from 2000 to 3500 masl in Colombia, Ecuador, Peru and Bolivia; from high plateau, which is cultivated in the surroundings of the Titicaca lake at more than 3500 masl; from halophyte soils, including cultivars highly tolerant to salinity; from sea level, which grows in central and southern Chile; and from subtropical or from Yungas which grows in low-altitude humid valleys in Bolivia (Padrón et al., 2014; Hinojosa et al., 2018). Depending on the characteristics of the genotype and of the phenological stage, quinoa is able to tolerate temperatures from -8 to 35 ºC and relative humidities from 40 to 88 % (Jacobsen et al., 2005). Of the countries that conform the Andes, Bolivia is the main producer, having destined 43,800 ha for the cultivation of quinoa in 2010 with an average yield of 1.8 t ha-1 (Jacobsen, 2011). Due to the diversity of habitats where it is cultivated, some ecotypes of quinoa are expected to be able to be developed with similar yields in North America or in other sites of the world. However, despite the wide adaptation that quinoa has in the Andes, temperatures higher than 35 ºC during flowering are the main limiting factor for the formation of seeds, which decreases the yield and represents the highest barrier for its expansion worldwide (Bazile et al., 2016; Hinojosa et al., 2018). Faced with this issue and due to the contribution of quinoa grains with food safety since they are gluten-free, have a high protein content (16 %) with a quality comparable to casein, iron, vitamins, antioxidants and amino acids such as lysine (Padrón et al., 2014; Zurita-Silvia et al., 2014; Wu et al., 2016), it is important to perform research where the effect of temperature on quinoa seeds germination is assessed, with the purpose of suggesting possible environments where its cultivation can be established.

Germination, which begins with the imbibition of the seed and finalizes when the radicle emerges, it is of great importance because it represents the first stage of the life cycle of a plant. The establishment of a crop depends on seeds germination that in turn is in accordance with temperature values (Nonogaki et al., 2010). For most of cereals, maximum germination occurs between 20 and 30 ºC, outside this range, values decrease significantly (Berti & Johnson, 2008). In seeds of Chenopodium quinoa Kamiri, Robura, Sajama and Samaranti var., the optimum germination (90%) occurs at 30 ± 2 ºC, but its range of temperatures with germinative capacity goes from 15 to 45 ºC (Bewley & Black, 1994; Boreo et al., 2000; González et al., 2017). In the proximities of minimum or basal temperatures and maximum or threshold ones, the number of germinated seeds decreases with regards to the optimum temperature that in addition, presents the higher germination rate. Basal, optimum and threshold temperatures are also called cardinal temperatures, outside of this range, germination does not occur (Windauer et al., 2007; Calzada-López et al., 2014).

Total germination, germination rate and cardinal temperatures are important since they can be taken as a reference for suggesting dates and locations for sowing with success possibilities. Mohamed et al., (1988) mentioned that the seeds germinated between 0 and 35 ºC will prosper in temperate zones, while the ones germinating between 10 and 45 ºC will develop in tropical zones (Caroca et al., 2016). In Chenopodium quinoa, Suyana and Tunkahuan varieties, studies implicating seeds germination at various temperatures have not been performed yet, which, although they would not solve the problem regarding their establishment in habitats beyond the Andes, they do contribute to the suggestion of establishment sites and dates for sowing. Therefore, the objective of this research was to evaluate the effect of various temperatures (5, 10, 15, 20, 25, 30, 35, 40, 45 and 50 ºC) on total germination, germination rate, average germination (t50) and cardinal temperatures of Chenopodium quinoa, Suyana and Tunkahuan varieties.

Material and Methods

Chenopodium quinoa seeds, Suyana and Tunkahuan varieties, were harvested during the springsummer 2017 cycle in the experimental field of the INIFAP, Texcoco de Mora, Estado de Mexico and donated for this research in February 2019. The seeds used for the test were separated and counted for making up the experimental units that consisted in a Petri dish of 100 x 15 mm, with two absorbent double paper disks moistened with 5 mL of distilled water and 100 seeds of Chenopodium quinoa Suyana or Tunkahuan varieties. The experimental design, with five replicates, consisted in 10 treatments or germination temperatures 5, 10, 15, 20, 25, 30, 35, 40, 45, and 50 ºC. For each variety, 50 experimental units were obtained and randomly distributed into each treatment. For the germination process, from imbibition to the emission of the radicle, five experimental units of each variety were placed in incubators under total darkness and adjusted to the temperatures of each treatment. The margin of error in each equipment was of ± 0.5 ºC. The following parameters were evaluated:

Total germination

In the experimental units of each treatment, the total number of germinated seeds was counted, considered as germinated when the emergence of the radicle had a length of ≥ 3 mm. The value in percentage was obtained with the equation proposed by Sampayo-Maldonado et al., (2017).


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Germination rate

The experimental units were examined every 2 h and, without replacement, the number of germinated seeds was counted. In the treatments from 15 to 40 ºC, the record ended when 6 h passed without emission of the radicle, in the treatments from 45 to 50 ºC when the seeds increased their volume and exploded when being touched and in the treatments from 5 to 10 ºC when they collapsed and hardened. Germination rate was obtained with the equation proposed by Calzada-López et al. (2014).


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Average germination or t50

In the Petri dishes of each treatment the number of hours passed since the imbibition of the seeds until 50 % of germination was reached, was registered. The TableCurve 2D v.3 Software was used for adjusting the sigmoid models and for obtaining the value of t50 for interpolation (Ordoñez-Salanueva et al., 2015).

Cardinal temperatures: basal temperature (Tb), optimum temperature (To), maximum temperature (Tm).

Basal temperature (Tb). With TableCurve 2D v.3 software, in the experimental units of each treatment, germination time of the Chenopodium quinoa seeds Suyana or Tunkahuan varieties was calculated in percentiles with intervals of 10. The inverse of germination time was graphed as a function of the temperature in order to observe the tendency of the data, locate the point of inflexion and determinate the suboptimum temperature. Then, a linear regression was performed to obtain the parameters of each percentile of germination (Ellis et al., 1986). The mean value of interception x (β0) was calculated and utilized for performing a second linear regression of each percentile of germination, another β0 was obtained, the mean average of both values represented the basal temperature of germination for each quinoa variety.

Maximum temperature (Tm). With TableCurve 2D v.3 software, suboptimum temperatures were determined, used to perform a linear regression to obtain the parameters of each percentage of germination. The mean value of β0 was obtained, with which the second linear regression was performed and the average value of β0 was obtained once again, which was the maximum temperature value (Hardegree, 2006).

Optimum temperature (To). Once basal and maximum temperatures were obtained, the equations of the second regression were equaled to zero. The value obtained was the optimum temperature (Hardegree, 2006).

Statistical analysis

A one-way analysis of variance and a comparison of means test (Tukey α ≤ 0.05) were applied to the values of total germination and germination rate, with SAS® v. 9.0 software for Windows. For their analysis, data in percentage were arcsin-transformed and returned to percentage for their description and discussion. TableCurve 2D v.3 software was used to obtain the values of t50 and cardinal temperatures.

Results and Discussion

Total germination

The total germination of Chenopodium quinoa Suyana was significantly higher (from 91 to 99.4 %) when seeds were exposed to temperatures between 15 and 35 ºC, while at 5, 10 or 40 ° C, the germination the percentages of germination oscillated from 73 to 87 % and were similar to each other. Nevertheless, with temperatures of 45 or 50 ºC, germination drastically decreased to 20.2 and 6.4 %, respectively. In Chenopodium quinoa Tunkahuan, germination was significantly higher, with values between 94 and 100 %, registered between 5 and 40 ºC and with 45 or 50 ºC, germination was of 40 %, with no differences induced by effect of the imbibition temperatures (Table 1).

Table 1.

Seeds of two varieties of Chenopodium quinoa imbibed at ten different temperatures.


Temperature (°C) Germination (%)
Suyana Tunkahuan
5 73.2 dz 94.2 a
10 87.4 bc 95.4 a
15 91.0 abc 97.2 a
20 92.2 ab 100 a
25 93.6 ab 98.6 a
30 99.4 a 95.6 a
35 94.6 ab 99.2 a
40 80.6 cd 95.0 a
45 20.2 e 42.8 b
50 6.4 f 36.6 b
HSD 10.6 10.7
CV (%) 6.7 5.9
z.

TFN1The means followed by different letters, in each column, indicate significant differences (Tukey, α ≤ 0.05). HSD, honest significant difference test; CV, coefficient of variation. Each data is the average of five replicates.


Between 5 and 40 ºC, the seeds of Chenopodium quinoa Tunkahuan had 94 % of germination, whereas at 45 or 50 ºC, the values were 2 or 6 times higher compared to Suyana seeds, whose germination at these temperatures was of 20.2 % and 6.4 %, respectively. The different responses to germination of these two varieties suggested that Tunkahuan could be cultivated in cold, temperate or warm areas, but not Suyana since its cultivation would be restricted to temperate and cold zones. Among different species or cultivars of the same species, the percentage of seeds germinated can vary with temperature, for instance, Steckel et al. (2004) mentioned that eight of nine species of Amaranthus have percentages of germination between 72 % and 82 % ºC at 30 °C, except Amaranthus blitoides which has a better response between 20 and 25 ºC. Physalis philadelphica seeds, Diamante, Chapingo and Tecozahutla cultivars had higher germination values than 80 % between 15 and 35 ºC, whereas P. philadelphica cv. Cerro Gordo had more restriction induced by effect of the temperature since the same percentage of germination was shown between 20 and 35 ºC (Calzada-López et al., 2014). In Chenopodium quinoa, the seeds belonging to Sajama, Santamaría or Titicaca cultivars have a germination ≥ 70 % when they are imbibed between 5 and 40 ºC. Particularly, seeds from Titicaca cultivar stand out because their germination is higher than 97 % from 5 to 35 ºC and it barely decreases to 88 % at 40 ºC (Mamedi et al., 2017). In the same interval of temperatures (from 5 to 40 ºC), seeds of Chenopodium quinoa Suyana, assessed in this research work, had a higher percentage of germination than the ones of Ch. Quinoa cv. Sajama or Santamaría, whereas the seeds of the Tunkahuan variety, which were also assessed in this research study, stood out from the other four, since even at 5 or 50 ºC its germination was of 94 and 37 %, respectively. Therefore, Chenopodium quinoa Tunkahuan can be considered as a viable option in a selection program of genotypes tolerant to extreme temperatures, with the condition that the temperature of the environment does not exceed 35 ºC during the flowering stage, otherwise, the panicle will not form grains (Hinojosa et al., 2018).

Germination rate.

The highest germination rate (7.4 seeds h-1) occurred at 30 ºC in Chenopodium quinoa Suyana, whereas Tunkahuan had its higher rate (6.6 seeds h-1) in the interval from 30 to 40 ºC. At 5 ºC, the germination rate decreased to 0.35 in both varieties, but at 50 ºC, it was 59 % lower in Suyana compared with Tunkahuan where 2.7 seeds h-1 germinated. In the range of temperature from 0 to 25 ºC, germination remained between 2 and 5 seeds h-1 regardless of variety (Figure 1).


[Figure ID: f1] Figure 1.

Germination rate of Chenopodium quinoa Suyana (A) or Tunkahuan (B). Each data is the mean of 5 replicates ± standard error. Different letters in each evaluation temperature indicate significant differences (Tukey, α ≤ 0.05).


Germination rate can change with the temperature of imbibition of the seeds and with the characteristics that each cultivar acquired during its process of domestication. For instance, in Physalis philadelphica, Diamante, Chapingo, Tecozautla or Cerro Gordo cultivars have a higher germination rate (17.3 to 21.6 seeds h-1) between 20 and 35 ºC, P. philadelphica Diamante always showing the highest values (Calzada-López et al., 2014). In researches performed with quinoa, Boero et al. (2000) mentioned that in seeds of Chenopodium quinoa Kamiri, Robura, Sajama and Samaranti varieties, placed onto Petri dishes at 8 ºC, germination rate fluctuated between 0.1 and 0.5 seeds h-1. A similar response was observed in Ch. Quinoa Suyana or Tunkahuan, at 5 ºC. On the other hand, Hinojosa et al., (2018) mentioned that in Andean cultivars of Chenopodium quinoa like Chucapaca, Surumi, Kamiri, Juganda and Jiwaki varieties, among others, germination rate decreased as temperature did, since 3 h were required, from imbibition, for viable seeds to germinate when exposed at 20 ºC, but the time was increased to 11 h when they were imbibed at 5 ºC and to more than 22 hours at 2 ºC. In this experiment, the time required for the germination of Ch. Quinoa Suyana or Tunkahuan seeds, exposed at 5 ºC, was of 122 h. The difference of 100 hours could be attributed to environment-induced preconditioning where Suyana or Tunkahuan varieties were developed (between 22 and 27 ºC), compared with cultivars of the Andean region that are developed with temperatures closed to 0 ºC.

Average germination (t50)

The seeds of Chenopodium quinoa Suyana placed between 20 and 35 ºC required, in average, 8.1 h to obtain t50, whereas the ones of Tunkahuan obtained it in 7.1 h and the range of temperatures was from 20 to 40 ºC. In both varieties the shortest times to obtain t50 were of 6 hours and occurred at 30 ºC. Below 20 ºC the time to obtain t50 was increased and above 40 ºC, average germination was not reached by any of the two varieties (Figure 2).


[Figure ID: f2] Figure 2.

Time required for middle germination or t50 at each temperature. Chenopodium quinoa (A) Suyana (5 °C, 143.5 ± 2.6 h; 10, 21.7 ± 2.6; 15, 18.7 ± 1.4; 20, 8.1 ± 1.3; 25, 8.6 ± 2; 30, 6.2 ± 1.5; 35, 9.5 ± 2.7; 40 °C, 14.7 ± 2.7 h). (B) Tunkahuan (5 °C, 138.2 ± 1.6 h; 10, 21.0 ± 2.9; 15, 17.1 ± 2.0; 20, 8.3 ± 1.5; 25, 7.7 ± 2.0; 30, 5.9 ± 1.1; 35, 6.1 ± 2.7; 40 °C, 7.3 ± 3.5 h); at 45 or 50 °C, t50 was not obtained for any variety.


Bois et al. (2006) mentioned that, for varieties of Chenopodium quinoa cultivated in the Andes such as Surumi, Kamiri and Juganda varieties, among others, the temperature needed for 100 % of germination to occur oscillates between 18 and 23 ºC. For Suyana or Tunkahuan varieties, whose seeds were harvested from plants that were developed between 22 and 27 ºC, 100 % of germination and the t50 values with shorter times were obtained at 30 ºC. The aforementioned suggests that the site where the crops are developed could precondition seeds so that their highest germination could occur at temperatures close to their development environment. During imbibition and reactivation of metabolism, stages I and II of germination, the exposure of seeds to low (≤ 5 ºC) or high (≥ 35 ºC) temperatures may cause death to the embryo, since events are affected, such as gibberellic acid synthesis or formation of mRNA participating in the activation of enzymes that degrade reserve compounds and translocate energy to the embryo (Bove et al., 2001; Rosa et al., 2004; Taiz & Zeiger, 2010). Seeds of Chenopodium quinoa Suyana or Tunkahuan exposed at 5 ºC, during stages I and II of germination, required 140 hours to reactivate their metabolism, obtain t50 value and final germination of 73 and 94 %, respectively. At 40 ºC, t50 values were 7.3 and 14.7 h, with final germination of 95 and 80 % for Tunkahuan and Suyana varieties, respectively. These results indicated that, in seeds of both varieties, the events occurring during stages I and II of germination were slowed down with low temperatures (5 ºC), but did not affect final germination, particularly in Tunkahuan variety. At the other end, high temperatures (≥ 40 ºC) significantly decreased germination, perhaps due to the denaturalization of cell or mitochondrial membranes participating in the generation of energy (ATP) for the reactivation of the embryo (Taiz & Zeiger, 2010). Moreover, seeds of the Suyana variety were more susceptible than Tunkahuan ones when exposed to high temperatures during the germination process.

Cardinal temperatures

In Chenopodium quinoa Suyana, the equations obtained for suboptimum and supraoptimum temperatures were: y = 0.006625X + (-0.022028); y = -0.009213 + 0.457407 and explained the variation of the germination rate in 86 and 65 %, respectively. For Tunkahuan variety, the equations and percentages with which the variation in germination rate could be explained were: y = 0.006178X + (-0.0175544), 93 %; y = -0.009213 + 0.457407, 81 %; corresponding to suboptimum and supraoptimum temperatures, respectively. Basal, optimum and maximum temperatures were: 2.3 and 1.8; 30.2 and 33.2; 48.8 and 62.2 ºC for Chenopodium quinoa Suyana and Tunkahuan, respectively (Figure 3).


[Figure ID: f3] Figure 3.

Germination rate in percentiles for each temperature in the range of cardinal temperatures of Chenopodium quinoa Suyana (A) or Tunkahuan (B). Tb, base temperature; To, optimal temperature; Tm, maximum temperature.


For a species or cultivar, the knowledge of the cardinal temperatures results important to predict its distribution areas with possibilities of success (Singh et al., 2008). The range of temperature where optimum germination occurs is unique in each cultivar and the exposure to suboptimum and supraoptimum temperatures could negatively affect seeds germination. However, those that maintain high percentages of germination at temperatures far from optimum might have a higher capacity to survive in warm or cold environments (Mamedi et al., 2017). In this case, basal and optimum temperatures were similar for both varieties, nonetheless, the maximum temperature was of 48.8 ºC for Suyana and of 62.2 ºC for Tunkahuan, suggesting that the crop of this last variety can be successful in warm or dry climates and that both of them can prosper in cold climates, as Sajama, Santamaría, Titicaca, Sayaña or Almida cultivars, which values of Tb go from -2 to 2 ºC (González et al., 2017; Mamedi et al., 2017).

In Chenopodium quinoa, the origin of the genotypes can be related to the germination temperatures of their seeds, for instance, in genotypes coming from three regions in Chile, those in the northern zone showed lower basal temperatures (9.4 ºC), but optimum (30 ºC) and maximum (50.6 ºC) temperatures higher than those in the central or southern zone, whose basal, optimum and maximum temperature were of 10.6, 27.8 and 44.9 ºC, respectively (Ayala-Pérez, 2018). Tm values higher in genotypes from the northern zone or Tarapacá region could be related with higher annual temperatures (from 11 to 19 ºC) that occur in this zone compared with the annual range (from 5.5 to 15.3) that occurs in O’Higgins or Los Lagos regions. In the case of Chenopodium quinoa Tunkahuan, the wide range (from 5 to 40 ºC) with germination ≥ 94 % and its maximum temperature from 60.5 to 63.8 ºC indicates that this variety can be cultivated and established in cold and temperate zones, but also in dry and warm zones such as in northern Mexico, whereas Suyana could be established better in temperate zones such as in central Mexico.

Conclusions

In temperatures ranging from 5 to 50 ºC, seeds of Chenopodium quinoa Tunkahuan had a higher capacity to germinate than those of Suyana.

In Chenopodium chinoa Suyana, the higher germination rate occured at 30 ºC, in Tunkahuan from 30 to 40 ºC.

In both varieties, germination slowed down at 5 ºC, whereas high temperatures (45 or 50 ºC) avoided reaching 50 % of germination.

Basal temperatures were similar in both varieties, but optimum and maximum temperatures were higher in Chenopodium quinoa Tunkahuan.

The wide ranges of temperatures at which seeds of Chenopodium quinoa Tunkahuan can germinate, indicated that they can be established, with possibilities of success, in cold, temperate or warm zones, whereas seeds of Suyana could be established only in cold and temperate zones.


fn1Cite this paper: Ramírez-Santiago, D., De-La-Cruz-Guzmán, G. H., Espitia-Rangel, E., Sampayo-Maldonado, S., Mandujano-Piña, M., Arriaga-Frías, A. (2020). Germination rate and cardinal temperatures in Chenopodium quinoa Suyana and Tunkahuan varieties. Revista Bio Ciencias 7, e880. doi: https://doi.org/10.15741/revbio.07.e880

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Revista Bio Ciencias, Año 12, vol. 8,  Enero 2021. Sistema de Publicación Continua editada por la Universidad Autónoma de Nayarit. Ciudad de la Cultura “Amado Nervo”,  Col. Centro,  C.P.: 63000, Tepic, Nayarit, México. Teléfono: (01) 311 211 8800, ext. 8922. E-mail: revistabiociencias@gmail.com, revistabiociencias@yahoo.com.mx, http://revistabiociencias.uan.mx. Editor responsable: Dr. Manuel Iván Girón Pérez. No. de Reserva de derechos al uso exclusivo 04-2010-101509412600-203, ISSN 2007-3380, ambos otorgados por el Instituto Nacional de Derechos de Autor. Responsable de la última actualización de este número Dr. Manuel Iván Girón Pérez. Secretaria de Investigación y Posgrado, edificio Centro Multidisciplinario de Investigación Científica (CEMIC) 03 de la Universidad Autónoma de Nayarit. La opinión expresada en los artículos firmados es responsabilidad del autor. Se autoriza la reproducción total o parcial de los contenidos e imágenes, siempre y cuando se cite la fuente y no sea con fines de lucro.

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