SciELO - Scientific Electronic Library Online

 
vol.26 número1La relación entre la calidad de vida, sentido de pertenencia y áreas verdes en ambientes urbanos en la ciudad de Durango, MéxicoCrecimiento radial de especies de pino en rodales sujetos a cortas de selección en Santa María Lachixío, Oaxaca, México índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • No hay artículos similaresSimilares en SciELO

Compartir


Revista Chapingo serie ciencias forestales y del ambiente

versión On-line ISSN 2007-4018versión impresa ISSN 2007-3828

Rev. Chapingo ser. cienc. for. ambient vol.26 no.1 Chapingo ene./abr. 2020  Epub 03-Mar-2021

https://doi.org/10.5154/r.rchscfa.2019.04.039 

Scientific note

Does the earthworm favor the survival and growth of Abies religiosa (Kunth) Schltdl. & Cham. seedlings in a nursery?

Lázaro R. Sánchez-Velásquez1  * 

Suria G. Vásquez-Morales1  2 

Rogelio Lara-González1 

Ángel I. Ortiz-Ceballos1 

María del Rosario Pineda-López1 

Guadalupe Hernández-Vargas1 

1Universidad Veracruzana, Instituto de Biotecnología y Ecología Aplicada (INBIOTECA). Av. de las Culturas Veracruzanas núm. 101, col. Emiliano Zapata. C. P. 91090. Xalapa, Veracruz, México.

2Universidad de Guanajuato, Departamento de Biología, División de Ciencias Naturales y Exactas. Noria Alta s/n, col. Noria Alta. C. P. 36050. Guanajuato, Guanajuato, México.


Abstract

Introduction:

In nurseries, irrigation inside plastic bags contributes to soil compaction, affecting plant growth.

Objective:

To evaluate the effect of the earthworm Pontoscolex corethrurus Müller on the survival and growth of Abies religiosa (Kunth) Schltdl. & Cham. plants and on soil compaction in a nursery.

Materials and methods:

The plants were subjected to three treatments (adult earthworm, two juvenile earthworms and no earthworms) in plastic bags (250 cc, 400 gauge) with 25 replicates. One year later, the height, cover, number of primary and secondary branches and biomass production (root, stems and branches) of the plants were recorded and soil compaction evaluated.

Results and discussion:

The earthworm promoted an increase of 28 % in height and 44 % in root dry matter production (P < 0.05) without affecting survival, which was similar (86 ± 4.25 %; P > 0.05) in all three treatments. Compaction was significantly lower (48 %, P < 0.0001) in the earthworm treatments.

Conclusion:

P. corethrurus has the potential to improve the quality of plants grown in plastic bags in forest nurseries.

Keywords: Pontoscolex corethrurus; sacred fir; soil compaction; plastic bags; plant quality

Resumen

Introducción:

En los viveros, el riego dentro de bolsas de plástico contribuye a la compactación del suelo, afectando el crecimiento de las plantas.

Objetivo:

Evaluar el efecto de la lombriz de tierra Pontoscolex corethrurus Müller en la supervivencia y crecimiento de plantas de Abies religiosa (Kunth) Schltdl. & Cham. y en la compactación del suelo en vivero.

Materiales y métodos:

Las plantas fueron sometidas a tres tratamientos (lombriz adulta, dos lombrices juveniles y sin lombriz) en bolsas de plástico (250 cc, calibre 400) con 25 repeticiones. Un año después, se registró la altura, cobertura, número de ramas primarias y secundarias y producción de biomasa (raíz, tallos y ramas) de las plantas y se evaluó la compactación del suelo.

Resultados y discusión:

La lombriz promovió 28 % de aumento en altura y 44 % de la producción de materia seca de la raíz (P < 0.05) sin afectar la supervivencia, la cual fue similar (86 ± 4.25 %; P > 0.05) en los tres tratamientos. La compactación fue significativamente menor (48 %, P < 0.0001) en los tratamientos con lombrices.

Conclusión:

P. corethrurus tiene potencial de mejorar la calidad de las plantas crecidas en bolsas de plástico en los viveros forestales.

Palabras clave: Pontoscolex corethrurus; oyamel; compactación del suelo; bolsas de plástico; calidad de planta

Introduction

In Mexico, Abies religiosa (Kunth) Schltdl. & Cham. (sacred fir) is distributed in the mountainous areas of Sinaloa, Chihuahua, Coahuila, Nuevo León, Tamaulipas, Hidalgo, Veracruz, State of Mexico, Tlaxcala, Puebla, Morelos, Jalisco, Michoacán, Guerrero and Oaxaca. The sacred fir, known as oyamel in Mexico, is a slow-growing species used as a Christmas tree (Pineda-López et al., 2015); its demand varies from 1.6 to 2.0 million, of which 60 % is destined for export to Canada and the United States of America (Zamora-Martínez, 2007).

Several types of containers are used in the mass production of nursery species, with one of them being plastic bags with soil as substrate (Allen, Harper, Bayer, & Brazee, 2017). In Mexico, they are widely used in government-promoted forest nurseries; in 2016, 2 761 443 plants were produced in these bags (Comisión Nacional Forestal [CONAFOR], 2017). Sacred fir seedlings are produced in these containers and remain in the nurseries for 18 to 24 months before being sent to plantations (CONAFOR, 2017). A disadvantage of plastic bags is that when irrigation is applied, some physical soil properties such as compaction are altered (Angst et al., 2017), which could affect plant survival and growth.

Earthworms have physical effects on soil structure (Angst et al., 2017; Brown et al., 2001; Scheu, 2003). Through their excavations, worms increase soil porosity and aeration (Datta, Singh, Singh, & Singh, 2016) and degrade organic wastes, which improves nutrient utilization by plants (Jansirani, Nivethitha, & Vijay, 2012; Pashanasi, Melendez, Szott, & Lavelle, 1992) and benefits their development (Eriksen-Hamel & Whalen, 2007). In addition, evidence indicates that worms benefit plant growth and productivity in arable or grassland soils (Ortiz-Ceballos & Fragoso, 2004). Pontoscolex corethrurus Müller is one of the endogenous earthworms that has demonstrated its effectiveness in soil improvement and crop productivity; moreover, it is common, easy to use and reproduce (Pashanasi, Lavelle, & Alegre, 1994), and is tolerant to extreme conditions (Cuevas-Vázquez, Vázquez-Luna, Martínez-Hernández, Gómez-López, & Ortíz-Ceballos, 2017).

Based on the above, the use of earthworms in the production of seedlings in plastic bags could increase soil porosity and aeration and improve the nutrient absorption of seedlings. This may be reflected in increased growth or biomass accumulation of the seedlings (dry weight). So far there is no evidence of the use of earthworms for the production of seedlings grown in plastic bags in greenhouses or nurseries. In this context, the objective of this research was to evaluate the effect of the earthworm P. corethrurus on the survival and growth of sacred fir seedlings, as well as on soil compaction. The hypotheses put forth were that the presence of the earthworm will allow for greater plant growth and significantly reduce soil compaction in plastic bags.

Materials and methods

Soil collection and experimental design

Approximately 100 kg of soil were collected from sacred fir forests in the El Conejo ejido, municipality of Perote (19° 31’54.5” N and 97° 09’ 14.8” W), located on the northwest face of Cofre de Perote, an inactive volcano in Cofre de Perote National Park, Veracruz Mexico. Tree density in these forests is 1 711.67 individuals·ha-1 (Pineda-López, Ortega, Sánchez-Velásquez, & Vázquez-Domínguez, 2013). The soil is classified as Andosol, which is susceptible to erosion (Instituto Nacional de Estadística y Geografía [INEGI], 2014). The soil of these sites has pH 5.79 ± 0.11 and total carbon, nitrogen and phosphorus percentages of 8.58 ± 0.84, 0.41 ± 0.037 and 0.27 ± 0.038, respectively (Perroni, Sánchez-Velásquez, Garza-Garza, Rojo-Alboreca, & Pineda-López, 2013). Uribe et al. (2012) indicate that these soil characteristics are appropriate for the growth of the earthworm P. corethrurus.

A composite sample was obtained from three samples extracted from five plots of 50 x 12.5 m (n = 15) at a depth of 30 cm in the rainy season (October 2008). The collected soil was mixed and remnants of roots and litter were excluded; it was then placed in black 250-cc, 400-gauge plastic bags. The size of the plastic bag used in this experiment is the same as that currently used in nurseries for the production of Christmas tree plants.

Open-pollinated seed from 10 cones of 10 trees (n = 100 cones) randomly chosen with a distance greater than 100 m between them was used. Scaleless seeds were deposited in wet river sand at 5 °C for eight days to promote germination (Young & Young, 2009). In the greenhouse, the seeds were placed on trays and covered with 3 mm of soil. The soil remained moist until germination, leaving the seedlings growing until the emergence of the first leaves (20 days). Subsequently, a month-old plant was placed in each plastic bag and the experiment was immediately started, consisting of three treatments: 1) an adult worm (1AW) with a developed clitellum, 2) two juvenile worms (2J) without a developed clitellum, and 3) control without a worm (NW). Juvenile worms reach maturity at approximately 60 days; two juveniles were used with the idea that at least one would reach maturity. Juvenile and adult worms weighed 0.011 ± 0.02 and 0.42 ± 0.05 g, respectively. Twenty-five replicates were used for each treatment; the bags for each treatment were chosen at random. The permanence of the worms in the experiment was observed through the soil removed on the surface of the bags. The earthworms were produced at Universidad Veracruzana’s Institute of Biotechnology and Applied Ecology. No pesticide or fertilizer was applied to the soil or plants. The experiment was carried out under nursery conditions with periodic watering, so that the soil was always kept moist (visual evaluation), which prevented the seedlings and worms from experiencing water stress; that is, the plant remained robust and with erect leaves.

At the end of the study (one year), when the seedlings reached the size to be sent to forest plantations (CONAFOR, 2017), the following records were taken: final height; diameter of average cover [(maximum + minimum) / 2]; number of primary and secondary branches; and dry matter of stem, branches, roots and total (sum of their parts). The dry matter was obtained by drying the plant parts at 60 °C until constant weight (72 h). Soil compaction was measured in each bag, at three randomly selected points, with a 0.635-cm-diameter pocket penetrometer, which is compaction-proof to 0.635 cm deep (Forestry Suppliers Inc. MPN: LR-280; UNSPSC: 41113910).

Data analysis

Survival was compared among treatments using a Chi-square test (χ2); that is, the sum of the squared differences of the observed values (number of individuals that survived in each treatment) minus the expected value (mean of the survivors of the treatments) divided by the expected value. Final height, cover, number of primary and secondary branches, dry biomass (stem, branches, roots and total) and combined variables such as the root:stem ratio and the proportion of biomass allocation to the root and aerial part (dry weight of stem and branches) were analyzed through ANOVAs with the SAS GLM procedure (SAS Institute Inc., 2016). All of them were used as response variables (dependent) and treatments (a factor) as a separate variable with three levels (1AW = one adult worm, 2J = two juvenile worms and NW = no worms). The transformed variables were final height (ln), cover area (sqrt; Zar, 2013), primary and secondary branches (ranks; Seaman, Walls, Wise, & Jaeger, 1994), root dry weight proportion (arcosin √root; Zar, 2013) and stem dry weight proportion (arcosin √stem). The variables dry weight of the stems, root, primary and secondary branches and total dry weight, as well as soil compaction and root:stem ratio did not require transformation. The normality of the data was checked with the Shapiro-Wilk test and the homogeneity of variances was analyzed with the Levene test. Multiple comparisons of means were made with Tukey’s test (P ≤ 0.05) when necessary.

Results and discussion

The initial height of the seedlings (4.42 ± 0.23 cm) was similar among the treatment groups (F = 1.74, P > 0.18, gl = 2, 72). At the end of the experiment, survival (86 ± 4.25 %) was similar in treatments with and without worms ( χ 2 = 0.84, P > 0.05). With respect to growth, the variables final height, root dry weight and soil compaction (Table 1; Figure 1) showed significant differences (P < 0.05). The 1AW treatment obtained the highest average height and root dry weight values. This same treatment and the 2J one showed the lowest soil compaction values, differing from the control (NW). There were no significant differences (P > 0.05) among treatments for the dry weight of the stem, primary and secondary branches and total, as well as for cover area, number of primary and secondary branches, r:s ratio and the dry weight proportion of the root and stem.

Table 1 Variables evaluated in Abies religiosa seedlings under Pontoscolex corethrurus treatments (1AW = one adult worm, 2J = two juvenile worms and NW = no worms) under nursery conditions.  

Variables ANOVA (GLM) Treatment Mean ± SE
Final height (cm) F = 3.62 P = 0.03 gl = 2, 62 1AW 2J NW 23.6 ± 1.60 a 22.0 ± 1.80 ab 17.0 ± 1.60 b
Root dry weight (g) F = 4.11 P = 0.02 gl = 2, 62 1AW 2J NW 0.54 ± 0.08 a 0.43 ± 0.06 ab 0.30 ± 0.04 b
Soil compaction (kPa) F = 13.29 P < 0.0001 gl = 2, 53 1AW 2J NW 63.0 ± 8.00 a 61.0 ± 8.00 a 128.0 ± 15.00 b
Stem dry weight (g) F = 2.37 P = 0.10 gl = 2, 62 1AW 2J NW 1.03 ± 0.12 a 0.82 ± 0.11 a 0.71 ± 0.08 a
r:s ratio F = 2.68 P > 0.07 gl = 2, 62 1AW 2J NW 0.45 ± 0.03 a 0.41 ± 0.02 a 0.36 ± 0.02 a
Root dry weight (%) F = 2.67 P > 0.07 gl = 2, 62 1AW 2J NW 30.32 ± 1.41 a 28.44 ± 1.22 a 26.21 ± 1.11 a
Stem dry weight (%) F = 2.67 P > 0.07 gl = 2, 62 1AW 2J NW 69.67 ± 1.41 a 71.56 ± 1.22 a 73.78 ± 1.11 a

r = root dry weight, s = stem dry weight (stem + branches). SE: standard error. The same letters in each variable indicate that there were no significant differences among treatments according to Tukey's test (P > 0.05).

Figure 1 Growth of Abies religiosa seedlings in plastic bags with Pontoscolex corethrurus (1AW = one adult worm, 2J = two juvenile worms and NW = no worms). The line at the top of each bar (treatment) indicates the standard error of the mean. Different letters on the bars indicate significant differences among means according to Tukey’s test (P < 0.05). 

The first objective in the production of nursery plants is to ensure survival. In this study, no significant differences in plant survival were obtained between the traditional treatment (NW) and the other two treatments applied (AW and 2J). Based on the literature reviewed, no studies have been published on the survival of plants associated with earthworms in forest nurseries using only soil and much less for A. religiosa or other conifers. For this reason, it is not possible to compare the results obtained in the present study; however, the 86 % survival obtained in this study may be acceptable in the production of plants for a period of one year. The second objective is the quality of the plant. Some of the attributes used to define plant quality are height, stem diameter and dry weight or combined variables (Poorter & Garnier, 2007). In this study, although stem diameter was not measured, other variables such as the number of primary and secondary branches and total plant cover area were considered. The variables height and root dry weight had significant differences among treatments (Table 1; Figure 1); the adult worm (AW) treatment reached the highest values. A higher allocation of biomass to the root could be associated with a greater gain in growth in the first years of life (Pike, Warren, & Montgomery, 2016). The year-long research experimentally demonstrated that earthworms favor the allocation of biomass to the root. This could be reflected in greater growth when plants are transplanted in the field for the production of Christmas trees, a situation that will have to be tested experimentally. Avendaño-Yáñez, Ortiz-Ceballos, Sánchez-Velásquez, Pineda-López, and Meave (2014) evaluated P. corethrurus and soil mixed with stubble from Mucuna pruriens var. utilis (Wall. ex Wight) Baker ex Burck or fertilizer versus no earthworms (control) in Quercus insignis M. Martens & Galeotti seedlings; the authors demonstrated that height, diameter, leaf biomass and total biomass were higher in treatments with worms. Other worms with positive effects have been used in crop plants; for example, Dichogaster bolaui Michaelsen in sorghum (Ávila, Bautista, Huerta, & Meléndez, 2010).

A combined variable that is also used to evaluate plant quality is the root:stem ratio, because it expresses how plants respond to the environment, primarily to light; the higher the root:stem ratio, the higher the quality of the seedling (Gregory, 2006; Pike et al., 2016). In this study, no significant differences were found among treatments (P = 0.07), possibly because all plants grew in the same shade level (30 %). In this regard, Saldaña-Acosta, Meave, and Sánchez-Velásquez (2009) demonstrated that seedlings of the same species and the same batch of seeds, grown in different shade levels, allocate different amounts of biomass to the root and stem. This underlines the importance of studying the root:stem ratio in nursery plants.

On the other hand, the presence of worms reduced soil compaction (Table 1; Figure 1). Worm burrows in the soil are associated with a reduction in bulk density and therefore in compaction (Joschko, Diestel, & Larink, 1989). The results agree with the reports of other studies carried out both in the field (Blanchart et al., 1999) and under controlled conditions (Joschko et al., 1989; Langmaack, Schrader, Rapp-Bernhardt, & Kotzke, 1999).

Benavides-Meza et al. (2016) assessed the growth of sacred fir plants from eight provenances (10 months and with the application of fertilizer) in smaller containers (93 cc) under greenhouse conditions and observed that the Cofre de Perote provenance achieved height growth of 22 ± 0.94 cm. Likewise, in the present study, the use of seeds from Cofre de Perote, but in much larger containers (250 cc), with earthworms and without fertilizers, achieved height growth (12 months) of 23.6 ± 1.6 cm. This suggests that the use of earthworms in larger containers has the potential to improve the quality of plants grown in forest nurseries, even without the application of fertilizer.

Conclusions

The presence of Pontoscolex corethrurus earthworms in plastic bags, for one year and under nursery conditions, significantly favors height growth and root dry weight of Abies religiosa plants. Similarly, earthworms reduce soil compaction caused by the application of irrigation to the plastic bag where the plant grows. This biotechnological process can contribute to the production of forest species by accelerating the growth of plants in nurseries, even without the application of fertilizers.

Acknowledgments

This project was funded by the National Council of Science and Technology (CONACYT) and the National Forestry Commission (CONAFOR) (Agreement 83060, CONAFOR-CONACYT C01-6163).

References

Allen, K. S., Harper, R. W., Bayer, A., & Brazee, N. J. (2017). A review of nursery production systems and their influence on urban tree survival. Urban for Urban Green, 21, 183-191. doi: 10.1016/j.ufug.2016.12.002 [ Links ]

Angst, Š., Mueller, C. W., Cajthaml, T., Angst, G., Lhotáková, Z., Bartuška, M., Špaldoňová, A., & Frouz, J. (2017). Stabilization of soil organic matter by earthworms is connected with physical protection rather than with chemical changes of organic matter. Geoderma, 289, 29-35. doi: 10.1016/J.GEODERMA.2016.11.017 [ Links ]

Avendaño-Yáñez, M. L., Ortiz-Ceballos, A. I., Sánchez-Velásquez, L. R., Pineda-López, M. R., & Meave, J. A. (2014). Synergic effect of Mucuna pruriens var. utilis (Fabaceae) and Pontoscolex corethrurus (Oligochaeta, Glossoscolecidae) on the growth of Quercus insignis (Fagaceae) seedlings, a native species of the Mexican cloud forest. Open Journal of Forestry, 4(1), 1-7. doi: 10.4236/ojf.2014.41001 [ Links ]

Ávila, M., Bautista, F., Huerta, E., & Meléndez, V. (2010). Evaluación del efecto del follaje de árboles forrajeros y oligoquetos en el crecimiento del sorgo en condiciones de invernadero. Acta Zoológica Mexicana, 26(2), 227-239. Retrieved from http://www.scielo.org.mx/pdf/azm/v26nspe2/v26nspe2a18.pdfLinks ]

Benavides-Meza, H. M., Gazca, G. M. O., López, L. S. F., Camacho, M. F., Fernández, G. D., de la Garza, L. M. P., & Nepamuceno, M. F. (2016). Variabilidad en el crecimiento de plántulas de ocho procedencias de Abies religiosa (H.B.K.) Schlecht. et Cham., en condiciones de vivero. Madera y Bosques, 17(3), 83-102. doi: 10.21829/myb.2011.1731144 [ Links ]

Blanchart, E., Albrechf, A., Alegre, J., Duboisset, A., Giloe, C., Pashanasf, B., Brussaard, L., & Lavelle, P. (1999). Effects of earthworms on soil structure and physical properties. In P. Lavelle, L. Brussaard, & P. Hendrix (Eds.), Earthworm management in tropical agroecosystems (pp. 149-172). UK: CABI International. [ Links ]

Brown, G. G., Fragoso, C., Barois, I., Rojas, P., Patron, J. C., Bueno, J., Moreno, A. G., …Rodríguez, C. (2001). Diversidad y rol funcional de la macrofauna edáfica en los ecosistemas tropicales mexicanos. Acta Zoológica Mexicana, 84, 79‒110. doi: 10.21829/azm.2001.8401847 [ Links ]

Comisión Nacional Forestal (CONAFOR). (2017). Abies religiosa (Kunth Schltdl. et Cham.). Retrieved from http://www.conafor.gob.mx:8080/documentos/docs/13/873Abies%20religiosa.pdfLinks ]

Cuevas-Vázquez, M. C., Vázquez-Luna, D., Martínez-Hernández, S., Gómez-López, O., & Ortíz-Ceballos, A. I. (2017). Sensitivity of the endogenic tropical earthwormPontoscolex corethrurusto the presence of heavy crude oil. Bulletin of Environment Contamination Toxicology, 99(2), 154‒160. doi: 10.1007/s00128-017-2126-2 [ Links ]

Datta, S., Singh, J., Singh, S., & Singh, J. (2016). Earthworms, pesticides and sustainable agriculture: a review. Environmental Science Pollution Research, 23(9), 8227‒8243. doi: 10.1007/s1135 [ Links ]

Eriksen-Hamel, N. S., & Whalen, J. K. (2007). Impacts of earthworms on soil nutrients and plant growth in soybean and maize agroecosystems. Agriculture, Ecosystems & Environment, 120(2-4), 442‒448. doi: 10.1016/j.agee.2006.11.004 [ Links ]

Gregory, P. (2006). Plant roots, growth, activity and interaction with soils. UK: Blackwell Publishing. [ Links ]

Instituto Nacional de Estadística y Geografía (INEGI). (2014). Conjunto de datos vectoriales perfiles de suelos. Escala 1:1 000 000. Aguascalientes, México: Author. [ Links ]

Jansirani, D., Nivethitha, S., & Vijay, P. S. (2012). Production and utilization of vermicast using organic wastes and its impact on Trigonella foenum and Phaseulos aurus. International Journal Research in Biological Sciences, 2(4), 187-189. Retrieved from https://pdfs.semanticscholar.org/3bd1/9c149b0a116bf244d9849417f3ee3329bc29.pdfLinks ]

Joschko, M., Diestel, H., & Larink, O. (1989). Assessment of earthworm burrowing efficiency in compacted soil with a combination of morphological and soil physical measurements. Biology and Fertility of Soils, 8(3), 191-196. doi: 10.1007/BF00266478 [ Links ]

Langmaack, M., Schrader, S., Rapp-Bernhardt, U., & Kotzke, K. (1999). Quantitative analysis of earthworm burrow systems with respect to biological soil-structure regeneration after soil compaction. Biology and Fertility of Soils, 28(3), 219-229. doi: 10.1007/s003740050 [ Links ]

Ortiz-Ceballos, A. I., & Fragoso, C. (2004). Earthworm populations under tropical maize cultivation: the effect of mulching with velvetbean. Biology and Fertility of Soils, 39(6), 438-445. doi: 10.1007/s00374-004-0732-8 [ Links ]

Pashanasi, B., Melendez, G., Szott, L., & Lavelle, P. (1992). Effect of inoculation with the endogenic earthworm Pontoscolex corethrurus (glossoscolecidae) on availability, soil microbial biomass and the growth of three tropical fruit tree seedlings in a pot experiment. Soil Biology and Biochemistry, 24(12), 1655-1659. doi: 10.1016/0038-0717(92)90165-T [ Links ]

Pashanasi, B., Lavelle, P., & Alegre, J. (1994). Efecto de lombrices de tierra (Pontoscolex corethrurus) sobre el crecimiento de cultivos anuales y características físicas y químicas en suelos de Yurimaguas. Folia Amazónica, 6(1-2), 5-49. doi: 10.24841/fa.v6i1-2.243 [ Links ]

Perroni, Y., Sánchez-Velásquez, L. R., Garza-Garza, S., Rojo-Alboreca, A., & Pineda-López, M. R. (2015). Variación estacional altitudinal de carbono, nitrógeno y fósforo en el suelo y su relación con la densidad del arbolado del bosque de Abies religiosa en el Parque Nacional Cofre de Perote. En M. R. Pineda-López, L. R. Sánchez-Velásquez, & J. C. Noa-Carrazana (Eds.), Ecología, biotecnología y conservación del género Abies en México: Estudios de Abies en México (pp. 61-80). Berlín, Alemania: Editorial Académica Española. [ Links ]

Pike, C. C., Warren, J. C., & Montgomery, R. A. (2016). Allometry of early growth in selected and wild sources of white spruce, Picea glauca (Moench) Voss. New Forets, 47(1), 131-141. doi: 10.1007/s11056-015-9498-0 [ Links ]

Pineda-López, M. R., Ortega, R., Sánchez-Velásquez, L. R., & Vázquez-Domínguez, G. (2013). Estructura poblacional de Abies religiosa (Kunth) Schydl. et Cham. en el ejido El Conejo del Parque Nacional Cofre de Perote, Veracruz, México. Revista Chapingo Serie Ciencias Forestales y del Ambiente, 19(2), 375-385. doi: 10.5154/r.rchscfa.2012.11.058 [ Links ]

Pineda-López, M. R., Sánchez-Velásquez, L. R., Vázquez-Domínguez, G., & Rojo-Alboreca, A. (2013). The effects of land use change on carbon content in the aerial biomass of anAbies religiosa(Kunth Schltdl. et Cham.) forest in central Veracruz, Mexico.Forest Systems,22(1), 82-93. doi: 10.5424/fs/2013221-02756 [ Links ]

Pineda-López, M. R., Sánchez-Velásquez, L. R., Perroni, Y., Gerez, P., López, C., & Rojo-Alboreca, A. (2015). The role of women in the forest conservation in a Mexican National Park: Pruning firs for the manufacture of Christmas wreaths. Human Ecology, 43(3), 493-501. doi: 10.1007/s10745-015-9756-y [ Links ]

Poorter, H., & Garnier, E. (2007). Ecological significance of inherent variation in relative growth rate and its component. In F. I. Pugnaire & F. Valladares (Eds.), Functional plant ecology (2nd ed., pp. 67-100). USA: CRC Press Taylor & Francis Group. [ Links ]

Saldaña-Acosta, A., Meave, J. A., & Sánchez-Velásquez, L. R. (2009). Seedling biomass allocation and vital rates of cloud forest tree species: responses to light in shade house conditions.Forest Ecology and Management, 258(7), 1650-1659. doi: 10.1016/j.foreco.2009.07.027 [ Links ]

SAS Institute Inc. (2016). Introducción a la programación en SAS® Studio 3.5. Cary, NC, USA: Author. [ Links ]

Seaman, J. W., Walls, S. C., Wise, S. E., & Jaeger, R. G. (1994). Caveat emptor: rank transform methods and interaction. Trends in Ecology and Evolution, 9(7), 261-263. doi: 10.1016/0169-5347(94)90292-5 [ Links ]

Scheu, S. (2003). Effects of earthworms on plant growth: patterns and perspectives. Pedobiologia, 47(5-6), 846-856. doi: 10.1078/0031-4056-00270 [ Links ]

Uribe, S., Huerta, E., Geissen, V., Mendoza, M., Godoy, R., & Jarquín, A. (2012). Pontoscolex corethrurus (Annelida: Oligochaeta) indicador de la calidad del suelo en sitios de Eucalyptus grandis (Myrtacea) con manejo tumba y quema. Revista de Biología Tropical, 60(4), 1543-1552. Retrieved from http://www.scielo.sa.cr/scielo.php?script=sci_arttext&pid=S0034-77442012000400012&lng=en&tlng=esLinks ]

Young, J. A., & Young, C. G. (2009). Collecting, processing and germinating seeds of wildland plants. Portland, USA: Timber Press. [ Links ]

Zamora-Martínez, M. C. (2015). Producción de árboles de Navidad. Revista Mexicana de Ciencias Forestales, 6(32), 4-5. Retrieved from http://www.scielo.org.mx/pdf/remcf/v6n32/2007-1132-remcf-6-32-00004.pdfLinks ]

Zar, J. H. (2013).Biostatistical analysis: Pearson new international edition. USA: Pearson Higher Ed. [ Links ]

Received: April 23, 2019; Accepted: October 28, 2019

*Corresponding author: lasanchez@uv.mx, tel.: +52 228 842 1700 ext. 10870.

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License