Revista Mexicana de Ciencias Forestales  Vol. 10 (55)

Septiembre –Octubre (2019)

Fecha de recepción/Reception date: 9 de mayo de 2019

Fecha de aceptación/Acceptance date: 9 de agosto de 2019

_______________________________

1Universidad Autónoma Chapingo, México

*Autor por correspondencia; correo-e: sebastian9477@gmail.com

Resumen

Las investigaciones sobre calidad de planta son necesarias para orientar la producción en vivero y contribuir a mejorar la supervivencia en campo de los individuos utilizados en programas de reforestación. Para indagar acerca del uso de variables morfológicas, fisiológicas y pruebas usadas en la determinación de la calidad de planta de especies nativas del género Pinus en México, producidas en vivero, se realizó una búsqueda de artículos científicos sobre el tema, publicados del año 2000 hasta mediados del 2018 en diferentes bases de datos. Se encontraron 61 artículos científicos (77 estudios). El diámetro y la altura resultaron ser los atributos morfológicos más utilizados, seguidos de la relación peso seco parte aérea entre peso seco de raíces. Respecto a los fisiológicos sobresalieron la concentración foliar de nutrientes y el potencial hídrico. En menos de un tercio de las investigaciones se llevó a cabo la comprobación de supervivencia en campo; por lo que, es importante aumentar el número de estudios respaldados con el uso de esta prueba, para dar mayor robustez y aplicabilidad a los resultados. Solo se han tratado, formalmente, 17 de los 57 taxones de pinos presentes en México. Dada la relevancia ecológica y económica del género, es importante continuar la investigación con los taxa faltantes, y profundizar en los ya considerados sobre temas como tipo de especies de hongos micorrícicos, su abundancia e intensidad de micorrización en las plantas, entre otros.

Palabras clave: Calidad de planta, estado del arte, índices de calidad, pinos, reforestación, viveros forestales.

Abstract

Research on seedling quality is necessary to guide nursery production and to contribute to the improvement of survival in the field in reforestation programs. In order to investigate the use of morphological and physiological variables as well as the tests used for determining the quality of seedlings of nursery-grown Mexican Pinus species, a review of the subject was carried out in scientific articles published between the years 2000 and mid-2018 in different databases. 61 scientific articles (77 studies) were found. Diameter and height were the most used morphological attributes, followed by the shoot:root ratio. The most used physiological traits were the leaf concentration of nutrients and the water potential. Less than one third of the research includes the performance of field survival tests; more studies should be supported using this test in order to render the results more robust and applicable. Only 17 out of the 57 pine taxa in Mexico have been formally researched. Given the ecological and economic relevance of the genus, it is essential to continue researching the other species and to delve further into such topics as the analysis of micorrhyzal species and the level of micorrhyzation in plants.

Keywords: Seedling quality, state of the art, quality indexes, pines, reforestation, forest nurseries

Introduction

Pine forests have a great ecological and economic importance in Mexico. They are often the main component of vegetation, influencing ecosystem processes, such as the hydrological and biogeochemical cycles; they are the habitat and source of food of wildlife, and they provide timber, firewood, pulp, resins, edible seeds and other non-timber forest products (Sánchez, 2008).

Mexico is a center of diversification of the genus Pinus, and in its territory includes the largest number of their taxa; this is caused, to a great extent, by orographic and climatic processes occurred in the geologic past (Challenger and Soberón, 2008). Gernandt and Pérez (2014) point out that the Mexican Republic hosts 57 of the approximately 120 taxa that make up the genus. According to the International Union for the Conservation of Nature (UICN, 2001), 35 species exhibited a status of least concern; seven are vulnerable; eight are close to being threatened; six are endangered, and one has an unknown status.

The Mexican nation is part of a global phenomenon  in which the pine forests are becoming fragmented and modified, mainly due to the introduction of non-native species, illegal logging, and the expansion of agricultural land and of forest fires (disturbed fire regimes) (Chapa et al., 2008; Ortíz et al., 2008; Bekele, 2011; Otavo and Echeverría, 2017). This renders the implementation of programs crucial to the conservation and propagation of the species at risk, as well as of those that are not at risk, through strategies for achieving a sustainable supply of germplasm or planting material (Broadhurst et al., 2015). This scenario generates the need for the production of plants in nurseries.

The establishment in the field of the produced individuals is limited by man-made factors, such as grazing, and by natural phenomena (frost and drought). In the case of the latter, they largely affect plant quality (Bautista et al., 2005; Robles et al., 2017; Prieto et al., 2018), which can be defined as the morpho-physiological characteristics of the plant that allow its survival, growth and development at the planting site (Duryea, 1985). Those characteristics that constitute an evidence of quality depend on genetics, but also on the propagation technology (Rodríguez, 2008; Prieto et al., 2009). The present work uses the term “seedling quality”; however, other terms have been utilized, as shown below.

The evolution of the concept of seedling quality was analyzed by Grossnickle and MacDonald (2018), who point out that the term has changed from “desirable seedlings”, i.e. seedlings selected based on their vigor and growth capacity, to “target seedlings”, i.e. seedlings with morphological and physiological characteristics that can be linked quantitatively to survival at the planting site (Mexal and Landis, 1990); all the way to the operational implementation of the latter concept and its expansion to “target plant” (including herbaceous shrub and tree species) (Landis, 2011) and its application in the relationship between nursery growers and reforesters, with the purpose of achieving specific reforestation goals (Dumroese et al., 2016).

Seedling quality is determined based on a series of morphological and physiological parameters, as well as on tests that help predict if individuals to be planted will survive. The most commonly used morphological attributes are the diameter (D), height (H), total dry weight (TDW), total fresh weight (TFW), dry weight of the aerial part (ADW), and dry weight of the roots (RDW). Indexes interrelating the above variables have been proposed, including the slenderness index (SI), the shoot:root ratio, Dickson’s index (DI) (Dickson et al., 1960), and the lignification index (LI). Commonly utilized physiological attributes are the water potential, the concentration of nutrients and non-structural carbohydrates (NSC), the net photosynthesis and the mitosis rate, among others. Also, there is evidence of behavior that includes the potential root growth (PRG) and resistance to cold and drought, among others (Duryea, 1985). There are quality intervals for the morphological attributes and certain physiological attributes of several Mexican conifer species, which allow classifying the quality of (cespitous and non-cespitous) pines and broad-leaved species, proposed by Sáenz et al. (2010) and modified by Rueda et al. (2014).

Numerous parameters have been included in the research on Mexican pines. However, there are no analyses of the frequency of use, nor of the success of each one of them or of the studied species. Based on the above, the objective of this literature review is to inquire about the use of morphological and physiological variables and of performance tests to determine the quality of nursery-grown native species of the genus Pinus in Mexico, with the purpose of carrying out a diagnosis and help perceive research opportunities on that topic.

Methodology

Literature search was conducted in the databases: ScienceDirect, Scopus, STOR, SciELO, Springer, Redalyc and Google Scholar. Literature was sought both in English and in Spanish, and the search was limited to scientific journal articles published between the years 2000 and mid-2018. No citations of previous years were included because they are practically non-existent. The words used were concentrated in title and keywords related to the nursery production of plants and in the plant quality of Mexican pine species; for example: quality, seedling quality, Pinus, Mexico, morphological parameters, physiological parameters, and survival. Given that some articles include more than one species, the research on each particular species was termed “study”.

Research and studied species

For the period under consideration, 61 articles were found, corresponding to 77 studies on the subject and the genus of interest, with an average of 4.3 per year. The variability was 0 (2006) to 8 (2015). Although there is no direct annual trend in the increase of publications, notably two thirds were published in the last 10 years (Figure 1).

Año = Year; Artículos publicados = Published articles

Figure 1. Published articles in scientific journals about plant quality of Mexican pines.

The hitherto published studies cover only 17 (29.8 %) of the 57 taxa that exist in Mexico. The most studied species, in descending order, are: P. pseudostrobus Lindl., P. greggii Engelm. ex Parl., P. hartwegii Lindl. and P. montezumae Lamb. (Figure 2). These four species account for 52 % of the reviewed studies, although Perry (1991) points out that several Mexican pine taxa have a great potential for use in commercial tree plantations.

Especie = Species; Número de estudios publicados = Number of published studies

Figure 2. Published studies in scientific journals by species.

Most of the studied species are of economic importance. Among the taxa that were not considered are those of lesser economic importance but with ecological relevance or with any level of risk of conservation; for example, Pinus attenuata Lemmon, P. contorta Douglas ex Loudon var. murrayana, P. jeffreyi Balf., P. maximartinezii Rzed., P. rzedowski Madrigal et M. Caball. and P. chiapensis (Martínez) Andresen, which are some of the 20 taxa included in the Official Mexican Standard of at-risk species (Semarnat, 2010), and regarding which further research is required for purposes of forest restoration.

In addition, there are studies on conservation and restoration that include the issue of seedling quality. Notably, the vast majority of the studies are directed to species that grow in a temperate-cold climate (94.6 %); only 4 % and 1.4 % refer to species of semi-arid regions and tropical, respectively; however, most of the national species correspond to the first type of climate.

Morphological variables and indexes

The most commonly used morphological variables are diameter (61 studies) and height (59 studies) (Figure 3). The morphological indicators for the 17 studied taxa are shown in Table 1.

D = Diameter, A = Height, PSR = Root dry weight, PSA = Shoot dry weight, PSA/PSR = Shoot:root ratio, PST = Total dry weight, ID = Dickson´s Index, IE = Height:diameter ratio, IL = Lignification Index.

Figure 3. Ratio of found studies per morphological variable (total number of studies: 77, in 60 articles).

Table 1 Morphological variables and indices in certain species of the genus Pinus.

*Species with grass stage. **Occasionally with grass stage. PP=Production type (C= Container; PB = Polyethylene bag). PT = Production period (months); Ref. = Reference(s): 1 (Prieto et al., 2004b); 2 (Prieto et al., 2007); 3 (Prieto et al., 2012); 4 (Prieto et al., 2018); 5 (Muñoz et al., 2015); 6 (Gutiérrez et al., 2015); 7 (Sáenz et al., 2014); 8 (Rueda et al., 2012); 9 (Bernaola et al., 2016); 10 (Rueda et al., 2014); 11 (Arteaga et al., 2003); 12 (Ávila et al., 2014); 13 (Rosales et al., 2015); 14 (Martínez et al., 2015); 15 (García et al., 2015); 16 (Barajas et al., 2004); 17 (Martínez et al., 2012); 18 (Sánchez et al., 2016); 19 (Bernaola et al., 2015); 20 (Palacios et al., 2017); 21 (Palacios et al., 2015); 22 (Buendía et al., 2017); 23 (Aldrete et al., 2002); 24 (Hernández et al., 2014); 25 (Aguilera et al., 2016a); 26 (Romero et al., 2012); 27 (López et al., 2018); 28 (Aguilera et al., 2016b); 29 (Ávila et al., 2017); 30 (Reyes et al., 2005). Note: The indicated intervals include the best recommended values in the references provided for each variable or index.

The review revealed other morphological variables and indices that were used to a lesser extent, such as: length of the main root (Ortíz and Rodríguez, 2008; Ávila et al., 2014; Robles et al., 2017), relative aerial dry weight and relative root dry weight (Sosa and Rodríguez, 2003; Robles et al., 2017), height/length of the main root ratio (Pineda et al., 2004; Sáenz et al., 2014; Muñoz et al., 2015), number and length of the root branches (Pineda et al., 2004), and volume of the root or shoot (Prieto et al., 2009; Bernaola et al., 2015, 2016; Prieto et al., 2018). As for the morphological indexes, the Root Container Index (ICR) is cited on two occasions (Bernaola et al., 2015, 2016). This is estimated by dividing the volume of the container (cm3) by the root volume (cm3). According to the last citation, the higher the value of the ICR (27.5 and 125.0), the higher the survival rate (13 and 94 %, respectively) in P. hartweggi plants two years after establishment in the field.

Diameter. Used in 79 % of the studies. A plant with good diameter is more likely to have adequate lignification, carbohydrate reserves, a greater amount of buds for resprouting, and a more developed root system (Rodríguez, 2008). For Mexal and Landis (1990), of all attributes, this is the most relevant, because it defines the robustness of the stem that is associated with the strength and the survival of the plantation. According to Sáenz et al. (2014), specimens produced in tubes or polystyrene trays with a diameter >5 mm are more resistant to bending and tolerate the damage caused by pests better, although this may vary depending on the species. However, these trends are not universal (Grossnickle, 2012).

Different diameters were observed for different taxa, according to the production period and technology in the nursery. Some examples of production in a container are P. hartwegii aged 12 months, with 5.1 mm (Bernaola et al., 2015); P. ayacahuite Ehrenb. ex Schltdl. aged 8 months, with 6.6 mm (Muñoz et al., 2015); and P. devoniana Lindl. aged 7 months, with 4.2 mm (Rueda et al., 2014). In the case of seedlings produced in polyethylene bags: P. montezumae aged 8 months with 11.2 mm (Aldrete et al., 2002) and 24 months, with 15.1 mm (Robles et al., 2017).

This information is for reference only, because the caliper is a feature that varies for the same species, due to such factors as the type and capacity of the container used (Bernaola et al., 2015), the source of the seeds (Ortega et al., 2003), the presence of micorrhyzae (Martínez et al., 2015), and the type of substrate (Arteaga et al., 2003), whether a shade mesh is utilized and the amount of time during which it is left over the crop, or whether or not it is a grass stage species, among other factors. The more adverse the plantation site is (with a higher moisture limitation, southern exposures, poor or degraded soils, etc.), the higher the value of this indicator should be, and vice versa: in more productive sites, it will tend to be lower. With bare rooted P. taeda L., South et al. (1985) found that the likelihood of mortality in the field above 75 % was 88 % in trees with a caliper of root neck of < 2.4 mm; however, as the caliper increased, the likelihood diminished, 8 % in those with a caliper of > 6.3 mm.

Height. The next most commonly utilized attribute was height, in 77 % of the studies. This feature has been used as a predictor of the quality of a plant, because it is a general measure of its photosynthetic capacity and transpiration, which is reflected in the development of the root structure and which eventually results in a better utilization of nutrients, water and anchoring (Mexal and Landis, 1990). A good height allows the plant to compete for growing space and to capture more solar radiation, compared to smaller plants (Grossnickle, 2012).

However, in adverse sites taller trees may have lower survival; while in favorable places these individuals achieve better survival rates. For example, Tuttle et al. (1988) found that, after 2 years of having been planted in productive sites, P. taeda trees exhibited an increased survival with respect to their height, up to 98 % in 35 cm tall specimens; conversely, in unfavorable sites, their mean survival was 55 %. Of course, for grass stage species, height is not a useful indicator.

P. pseudostrobus produced in containers records heights of 27.9, 24.3 and 29.4 cm at 9, 10 and 12 months, respectively (Sáenz et al., 2014; Aguilera et al., 2016b; Ávila et al., 2017), and P. hartwegii, heights of 16.11 and 34.8 cm, at 12 and 24 months (Viveros et al, 2007; Bernaola et al., 2015). In the traditional production system in polyethylene bags, P. greggii has been observed to reach a height of 24.9 cm at 10 months (Barajas et al., 2004).

Dry weights and shoot:root ratio. The SDW was determined in 53 % of the reviewed studies, and the RDW, in 55 %. The reason for determining the weight on a dry matter basis is because the amount of water in the plant tissue can vary greatly, and therefore the fresh weight provides a less consistent measurement than the dry weight (Haase, 2007). As for the TDW, it is cited in 43 % of the studies. A quality plant should be as heavy as possible in order to produce the best growth, without losing the balance between the shoots and the roots required for its survival (Thompson, 1985). In addition, it has been proven that there is a strong relationship between the dry weight of plants and their stem diameter (Ritchie, 1984), and therefore, it correlates with the survival and growth in the field.

The shoot:root ratio provides more information than the individual dry weights and was determined in 51 % of the studies. A quality plant must have a low shoot:root ratio in order for its chances of survival to increase; since a well-developed root structure will allow a better absorption of nutrients, as well as a better accessibility to water. In this review we identified values ranging between 0.2, in P. pseudostrobus produced in bag (Aldrete et al., 2002), and 3.2 to 6.1, in P. engelmannii Carrière grown in containers (Rosales et al., 2015; García et al., 2015). Rueda et al. (2014) recommend a value of <2.0.

Dickson’s Index. DI relates the variables diameter, height and shoot:root ratio, and adjusts them according to the size of the plant (TDW). Higher values represent a good, balanced development of the plant (Reyes et al., 2005). According to Rueda et al. (2014), plants with a DI > 0.5 are of good quality; in the present review, the obtained values ranged between 0.07 for P. engelmannii (Rosales et al., 2015), and 4.7 for P. montezumae, a cespitous species, produced in a bag (Robles et al., 2017).

Slenderness Index. The SI is the relationship between the height and diameter of the plant; the lower its value, the lower and thicker the plant will be, and therefore, the more suitable for environments with limitations of moisture or cold (Rodríguez, 2008). Roller (1977) proved that a slenderness index below 6.0 is associated with a better quality of individuals of Picea mariana. In the consulted literature, the values ranged between 1.6 for P. devoniana at 7 months of age (Rueda et al., 2014) and 10.4 for P. greggii at 9 months (Sáenz et al., 2014). If the index is high during the cultivation, aerial pruning is recommended; it is equally recommended when the shoot:root ratio has high values, in order to compensate transpiration with water absorption.

Lignification Index. The lignification index, cited in 6 % of the studies, provides an estimate of the degree of robustness that is needed for the plant to resist the stress, including hydric stress, at the planting site (Prieto et al., 2009). Values of 29.2, 22.9 and 24.3 % were registered for P. engelmannii when assessing the reduction in moisture availability as a form or preconditioning (Prieto et al., 2004a; Ávila et al., 2014); in P. leiophylla Schiede ex Schltdl. et Cham., the value was 30.9 %, considering the substrates and the nutrient addition rates (Buendía et al., 2017). Although this index can be a useful estimate, the wet weight of a plant is not a very accurate measure, as we mentioned before.

Physiological variables

Concentration of nutrients. The study of the concentration of nutrients has focused mainly on nitrogen (36.4 % of the total of studies), phosphorus (32.5 %), and potassium (28.6 %) (Figure 4) (Table 2). It is important because it assesses one of the most critical components in high-quality nursery production: fertilizers (Jacobs and Landis, 2009). According to these authors, plants require adequate amounts of nutrients in order to keep the balance of their basic physiological processes, like photosynthesis, and to promote rapid growth and development. Without a good supply of nutrients, growth becomes slow, which reduces the vigor of the plant. A good fertilization promotes better growth rates. However, an excess of nutrients can affect the optimal development of individuals and even render them toxic; therefore, it is useful to measure the concentration of nutrients as an estimator of quality (Gutiérrez et al., 2015). Another negative effect of abundant fertilization with N, in the area of superfluous consumption, is that it promotes the synthesis of cytokinins, leaf development, and a low root development, as well as limited availability of carbohydrates; as documented by Rodríguez et al. (2002) for the bare-root production of P. palustris Mill. in the Southeast of the United States of America.

Frecuencia = Frequency; Variable fisiológica = Physiological variable; Concentración de nitrógeno = Nitrogen concentration; Concentración de fósforo = Phosphorus concentration; Concentración de carbono = Carbon concentration; Concentración de lignina = Lignin concentration; Potencial hídrico = Water potential; Crecimiento potencial de raíz = Potential root growth; Concentración de carbohidratos = Carbohydrates concentration

Figure 4. Frequency of the found studies per physiological variable.

Table 2. Some physiological indicators in Pinus species.

PT = Production type (C=container, PB = Polyethylene bag). PP = Production period. Ref.=Reference(s). References: 31 (Ortega and Rodríguez, 2007); 32 (Gómez et al., 2013). †Standard values for nutrients in the leaf area of seedlings produced in containers (Landis, 1989). Note: The indicated intervals include the best values recommended in the references for each variable or index.

Each nutrient performs specific functions in the physiological processes of the plant; therefore, quantification of the nutrients helps establish its quality (Jacobs and Landis 2014). However, only four studies analyzed secondary macronutrients and micronutrients; notably, three of them refer to the use of ectomicorrhyzal fungi (Martínez et al., 2012; Rentería et al., 2017; Barragán et al., 2018); one evaluates the effect of two levels of pH of irrigation water, and two assess the effects of fertilization on the morphology and leaf concentration of nutrients of P. cembroides Zucc. (Gutiérrez et al., 2015).

In certain studies, the levels of N, P and K are below or above those proposed by Landis (1989) for conifers produced in containers. However, most of them declare a good plant quality, without visible responses of deficiency or excess of nutrients. This suggests that, in the face of the diversity of forest species in Mexico, the suggested concentrations of nutrients are a good starting point which, nevertheless, must be adjusted, often by reducing them.

Concentration of carbohydrates. Only two studies (2.6 %) were found for this variable in P. greggii (Cetina et al., 2001; Cetina et al., 2002). These authors compared the response to aerial and root pruning treatments, as well as to irrigation regimes, in the storage of soluble sugars and starch. Both studies emphasized the importance of the accumulation of NSC as reserves that are essential for survival, especially in the face of adverse conditions. The NSC play a role in the processes of energy transportation, metabolism and osmoregulation, and as a raw material in the synthesis of defense compounds and exchange with micorrhyzae in nutrient acquisition; and despite their prominence in the functionality of the plant, the understanding of the dynamics of their storage, controls and response to environmental stress are very limited; therefore, further research in this field is required (Marshall, 1985; Hartmann and Trumbore, 2016).

Water potential (Ψw). Used in 7.8 % of the studies. This indicator (whose numerical value is equal to that of hydric stress, but with the opposite symbol) is a measure of free energy or chemical potential of water and consists mainly of two components in a plant nursery: osmotic potential (Ψo) and the potential for pressure (Ψp) (Landis et al., 1989).

It is usually expressed in MPa. In general, a plant exhibits moderate to very high stress when its value corresponds to a range of -1.0 to -2.5 MPa (Ritchie et al., 2010). It is important to know the levels of stress that each species can tolerate, in order to avoid failure of the restoration programs. A clear example of this is the use of P. leiophylla as a pioneer species that can resist a stress of up to -3.5 MPa (Castelán, 2014).

Despite being a good predictor of drought resistance in field, the Ψw is very dynamic and can be affected by environmental conditions, the species and its provenance, the level of rest, the level of stress resistance and the age of the plant (Haase, 2007). Thus, the Ψw would reflect the quality of the plant only when stress is moderately high and is maintained during several days (Ritchie et al., 2010). Given this situation, there are other tests, such as the analysis of xylem susceptibility to cavitation, the stability of the cell membrane or photochemical efficiency, which may provide more information on the levels of water potential that a plant can attain before its physiological functioning becomes irreversibly damaged or affected.

Performance tests

Performance tests or performance attributes are determined by placing samples of plants in controlled environments and evaluating their specific responses. They have the inconvenience of being time consuming; however, they yield results in terms of the responses of the plant that often relate to its performance in the field (Ritchie, 1984). Resistance to cold and root growth potential, cited in only 1 % and 5 % of the studies, respectively, are among the most widely used tests in the world today.

Resistance to cold. It refers to the minimum temperature at which a percentage of a population of seedlings will survive or maintain a given level of damage (Ritchie, 1984). In temperate and cold areas, resistance to cold occurs naturally and is expressed through the hardening of the plant; however, when seeking to produce the plant in a nursery, it is necessary to understand the process of resistance to cold in order to obtain a properly hardened material (Glerum, 1985).

The only case, among the revised articles, in which this variable was used was that of Ramírez and Rodríguez (2010), who applied different concentrations of potassium nitrate during the hardening stage to nursery-grown Pinus hartwegii plants, which reached an age of 13 months. The likelihood of damage by cold after a frost (-5 °C by 2 h), simulated in a controlled environment chamber, was modeled. The damage was determined visually, although there are other methods to assess the resistance to cold, such as the loss of electrolytes test (Dexter et al., 1932; McKay, 1992; Burr et al., 2001) and the measurement of chlorophyll fluorescence (Vidaver et al., 1988). Finally, some authors have shown the effect of cold directly in the field. An example is the case of Viveros et al. (2007), who used this modality to prove that there may be intraspecies variations in tolerance to cold.

Root growth potential. Only three studies used it (3.9 % of the total). Sánchez et al. (2016) transplanted Pinus oaxacana and P. greggii seedlings into pots with a capacity of 10 L, with a substrate of bark (70 %) and perlite (30 %). The specimens were kept during 28 days in the greenhouse and were watered every day; at the end of this period, 17 and nine roots, respectively, were registered. Ávila et al. (2017) used the same methodology, but during 40 days, with P. oaxacana.

On the other hand, Robles et al. (2017) transplanted P. montezumae seedlings into pots of 4 L with a different substrate and watered them every other day during one month. These authors correlated survivals above 80 % with an average of 55 new roots; it was concluded that the test is good for estimating survival based on the ability of the plants to issue roots, given that, in general, it conveys an idea of the functionality of various physiological systems (Ritchie et al., 2010). However, it has also been widely discussed, because its accuracy is restricted to species that produce abundant roots and grow under unlimiting environments (Simpson and Ritchie, 1997; Oliet et al., 2003; Ritchie and Landis, 2003).

Nursery factors

The seedling quality can be affected by many factors; therefore, the nursery grower should ensure an appropriate combination of biotic and abiotic factors in order to achieve a good seedling quality. In this regard, various researches have focused on assessing the direct effect of these aspects through the years. In this review, the recurrence of such variables as the type and size of the container, the substrate used, the applied fertilizers, the applied preconditioning, and others like the type of pruning and the use of micorrhyzae was notorious. In general, it was demonstrated that the use of containers of greater capacity improves the root developments and plant quality (Prieto et al., 2007; Bernaola et al., 2015). On the other hand, the substrate utilized in the different researches was peat moss, due to its ideal physicochemical properties (Li et al., 2009); however, it was observed that in most of the studies, the proposed alternative substrates produced similar or superior results to those of peat moss (Reyes et al., 2005; Hernández et al., 2014; Aguilera et al., 2016a; Aguilera et al., 2016b). In addition, the usefulness of controlled release fertilizers and of preconditioning as a way of contributing to improve the quality of the plants prior to their establishment in the field was proven (Prieto-Ruiz et al., 2004a, 2004b).

Verification of in-field survival

The vast majority of the reviewed studies used only morphological parameters as indicators of the quality of a plant. This may be due to the difficulty of access to expensive equipment and instruments to perform the physiological tests, as well as to the need for trained personnel. Or else, there may be a lack of financial resources to cover the costs in the laboratories that carry out this kind of determinations.

The physiological indicators should not be considered without taking into account the morphological characteristics, for a plant may have good nutrition, but if its root system is not well developed, the likelihood that it will survive in an environment with moisture limitations is low (Rodríguez, 2008; Gutiérrez et al., 2015).

Only in 29.5 % of the reviewed articles (Table 3) was a survival test performed, and given that the definition of plant quality involves survival, the subsequent studies must carry out in-field verifications, which will provide them with greater robustness and scientific rigor.

Table 3. Peer-reviewed studies on the assessment of survival in the field.

AP=Assessment period (months), EI=Evaluation of increases in morphological variables. Ref.=Reference, S=survival, D=diameter, H=height. References: 33 (Cetina et al., 2002), 34 (Díaz  et al., 2012), 35 (Ortiz and Rodríguez, 2008), 36 (Ramírez and Rodríguez, 2009), 37 (Bautista et al., 2005), 38 (Robles et al., 2017), 39 (Sosa and Rodríguez, 2003), 40 (Sigala et al., 2015).

Conclusions

Most of the research uses morphological parameters —primarily height and diameter— as indicators of quality. Yet, although the diameter is a good indicator, the use of physiological parameters allows to better understand the operation of the plant both in the nursery and at the planting site.

There is room for further inquiry in relation to the physiological attributes, such as the reserves of carbohydrates, fluorescence of chlorophyll, and the loss of electrolytes, in the determination of seedling quality. In addition, performance tests such as the dormancy of the bud for species of cold environments, resistance to stress (due to drought or frost) and proof of root growth potential should be implemented more often.

In the future, more research must be supported with evidence of survival in the field in order to provide greater robustness and applicability to the results.

Few Pinus taxa are studied. It is important to deepen in the research that is yet to be carried out, but it is equally necessary to expand the range of species, if we are to have an impact and to incorporate restoration programs including taxa at risk and other taxa of economic or ecological interest.

The names of plant quality indicators need to be standardized in Mexico and in the Spanish language. In nursery studies, there is a recurrence of factors such as the type and size of the container, the utilized substrate, the applied fertilizers, and the applied preconditioning, among others. In general, it was observed that the use of containers of greater capacity improves the root development and plant quality. Peat moss is the most commonly used substrate in various researches; however, similar or superior results to those of peat moss were obtained with alternative substrates. The usefulness of controlled release fertilizers and of preconditioning as a way of contributing to improve the seedling quality prior to their establishment in the field has been proven.

Conflict of interests

The authors declare no conflict of interests.

Contribution by author

Sebastián Escobar-Alonso: collection, organization and analysis of the information; Dante Arturo Rodríguez-Trejo: research conception, organization and analysis of the information. All the authors participated in writing and implementation of the observations to the document.

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