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Introduction
Artificial forest repopulations in Mexico have low productivity and survival, which is less than 50 % after one year of establishment and decreases in subsequent years (Vargas & Venegas, 2012). Selection of plants not adapted to the environment and low water availability are important factors that limit the success of reforestation (Burney et al., 2015).
Vegetation establishment is subject to plant quality, environmental conditions and site preparation, but water availability is the most limiting factor (Burney et al., 2015). Plants use mechanisms to adapt to a water deficit that differ between species and among their geographical provenances; for example, those belonging to arid sites show greater water-use efficiency (Cregg, Olivas-García, & Hennessey, 2000). These adaptations make it possible to select species or provenances with greater survival abiliity in dry areas or with changes in soil moisture (Martínez-Trinidad, Vargas-Hernández, López-Upton, & Muñoz-Orozco, 2002).
Pinus cembroides Zucc. and P. orizabensis D. K. Bailey and Hawksworth (Bailey & Hawksworth, 1992; Luna-Cavazos, Romero-Manzanares, & García-Moya, 2008) are two pine species that inhabit semi-arid areas of Mexico. Both present a pink edible embryo that provides food and economic benefits to their owners (Hernández, Islas, & Guerra, 2011; Perry, 1991). Pinus cembroides is the most widely distributed Mexican pinyon pine, ranging from the southern U.S. to Querétaro, Hidalgo and northwest Veracruz, at an elevation of 1 700 to 2 400 m (Bailey & Hawksworth, 1992; Perry, 1991). Pinus orizabensis is endemic to the states of Puebla, Tlaxcala and central-western Veracruz, below 20° North latitude; it is part of the transition vegetation between temperate forests and xerophilous scrub (Granados, Granados, & Sánchez, 2015; Perry, 1991) and inhabits heights from 2 300 to 2 700 m (Bailey & Hawksworth, 1992). Both species are affected by overgrazing, mainly by goats, overexploitation in the pine nut harvest and the expansion of the agricultural frontier.
The two species are very similar, although Bailey and Hawksworth (1992) point out differences in mature trees, and Hernández-Anguiano, López-Upton, Ramírez-Herrera, and Romero-Manzanares (2018) distinguish them at the seedling level. However, being physically separated causes confusion and they are collected indistinctly for reforestation programs. By establishing reforestation with the wrong species or provenance, the natural distribution, development and survival of the plants are altered due to adaptive differences, for example, to water deficit (Espinoza, Magni, Santelices, Ivković, & Cabrera, 2016).
The species are not sympatric, since they have differences in their elevation intervals (Bailey, 1983; Bailey & Hawksworth, 1992), which suggests adaptive differences between them. In this context, the objective of the present study was to determine drought resistance in seedlings of three provenances of P. cembroides and three of P. orizabensis, through growth in height, diameter and aerial and root biomass production as a response to water deficit.
Materials and methods
The germplasm was obtained in natural P. cembroides and P. orizabensis stands in 2014 and 2015. Cones were collected from 15 vigorous, healthy trees per population, located at a distance of more than 50 m between them. The seed was sown on January 15, 2016 in 330 cm3 plastic tubes. The substrate was made from composted pine bark, sawdust and perlite at a ratio of 1:1:1, to which slow-release fertilizer (7 kg·m-3; Nutricote® 17-7-12) was added. The plants were kept in normal irrigation for 16 months. The irrigation-drought experiment began on May 30, 2017 with six provenances, three of each species (Figure 1), in the Colegio de Postgraduados’ Postgraduate Forest Sciences greenhouse (19° 27’ 38.25” N and 98° 54’ 23.91” W, at 2 240 m) in Texcoco, State of Mexico, Mexico. During the experiment, the average temperature was 16.5 °C.
The location of the provenances was obtained with a Garmin® Etrex 10 Datum WGS84 geopositioner, and the average annual temperature and precipitation were obtained with the ANUSPLIN software (Sáenz-Romero, 2011) (Table 1).
Table 1 Location and characteristics of the provenances of Pinus cembroides and P. orizabensis included in this study.
| Provenances | N latitude | W longitude | Elevation (m) | Temperature (°C) | Precipitation (mm) |
|---|---|---|---|---|---|
| Pinus cembroides | |||||
| El Carrizal, Colón, Querétaro | 20° 52' 40" | 100° 05' 07" | 2 159 | 16.0 | 626 |
| La Laja, Cadereyta, Querétaro | 20° 48' 44" | 99° 38' 19" | 2 831 | 14.2 | 890 |
| La Florida, Santiago de Anaya, Hidalgo | 20° 28' 36" | 98° 59' 02" | 2 002 | 17.3 | 511 |
| Pinus orizabensis | |||||
| Tepeyahualco, Tepeyahualco, Puebla | 19° 30' 26" | 97° 30' 26" | 2 417 | 13.8 | 491 |
| Rancho Domínguez, El Carmen, Tlaxcala | 19° 24' 01'' | 97° 42' 44'' | 2 671 | 13.1 | 565 |
| Las Cuevas, Altzayanca, Tlaxcala | 19° 22' 44" | 97° 43' 02" | 2 479 | 14.0 | 573 |
In each population, the plants were selected in such a way that they had a homogeneous size (Martiñón-Martínez, Vargas-Hernández, López-Upton, Gómez-Guerrero, & Vaquera-Huerta, 2010). They were transplanted into 10 cm diameter and 100 cm long PVC pipes in order not to limit root growth. The substrate was made up of composted sawdust and tepezil (pumice) waste material at a 1:1 ratio; the mixture was previously sterilized at 90 °C for 5 hours. No fertilizer was added to the substrate to avoid interaction with stress tolerance (Villar-Salvador, Peñuelas, & Jacobs, 2013). The substrate pH was 6.6, electrical conductivity was 1.5 dS·m-1, organic matter content 14.4 %, nitrogen 0.13 %, phosphorus 0.01 mg·kg-1, sodium 0.08 cmol(+)·kg-1 and potassium 0.15 cmol(+)·kg-1.
A split-plot experimental design consisting of two moisture environments (irrigation and drought) with replicates (blocks) nested within them was used; in each block, the six provenances (three per species) with 10 plants per experimental unit were assessed. In total there were 240 plants per moisture environment. Another 136 tubes with plants were placed as an experimental barrier. To define the moisture levels to be evaluated, the field capacity (0.03 MPa) and the permanent wilting point (1.5 MPa) were determined. The irrigation timing was determined using the gravimetric method. In the irrigation condition, the moisture level was kept between 38 to 45 %, while in the drought condition it fluctuated from 30 to 36 %. The water was replenished when the minimum moisture allowed for each treatment was reached, a condition that remained for 11 months.
Variables evaluated
At the beginning (16-month-old plant) and end of the experiment (27-month-old plant), height, diameter and presence or absence of secondary leaves were determined. In addition, the number of branches was counted and the initial root length was measured using a graduated ruler (mm) and a Mitutoyo digital vernier caliper (approximation in mm). The difference between the initial and final values of the growth variables was considered as the increase in each of them. The percentage of secondary leaves was calculated with the proportion of plants with secondary leaves and an average value per plot was used. Likewise, at the beginning and end of the experiment, 40 plants of each provenance and treatment were sampled, separating the aerial part (stem, leaves and branches) and the root to determine the respective biomass. The root system was carefully washed; subsequently, the aerial part and the root were separately deposited in paper bags and placed in a drying oven at 70 °C until constant weight. The needles of the twigs were separated from the aerial part and weighed separately on an analytical balance.
Statistical analysis
A joint analysis of variance of the two moisture conditions was performed with the SAS version 9.0 (Statistical Analysis System [SAS Institute Inc. ], 2003) MIXED procedure. For the variables in which the individual data per plant were used, the following linear model that corresponds to a split-plot experimental design was used:
where,
Yijklm |
value observed in the mth individual of the lth provenance within the kth species, in the jth block nested in the ith moisture environment |
µ |
population mean |
Si |
fixed effect of the ith drought level |
Bj(i) |
random effect of nested block on drought level ~NID (0, σ2 B(S)) |
Ek |
fixed effect of the kth species |
SEik |
fixed effect of drought level interaction by species |
BEj(i)k |
random effect of block-by-species interaction ~NID (0, σ2 BE) |
Pl(k) |
fixed effect of the lth provenance within the kth species |
SPil(k) |
fixed effect of the drought level interaction by provenance within species |
BPj(i)l(k) |
random effect of the nested block interaction on the drought level by provenance within species ~NID (0, σ2 BP) |
eijklm |
sampling error within plots ~NID (0, σ2 e): i = irrigation and drought; j = 1, 2, 3 and 4 blocks; k = P. cembroides and P. orizabensis; l = 1, 2 and 3 provenances per species; m = 1, …10 plants per plot. |
A similar reduced model (i. e., not including sampling error within plots) was used for the percentage of secondary leaves, as the values were obtained per plot.
Mean separation was done by direct comparisons between pairs of means with the SAS (2003) MIXED procedure; a P < 0.05 significance level was considered in all analyses.
Results and discussion
Response of morphological variables to water deficit
The variables increase in height and diameter, root length and number of branches showed significant differences (P = 0.0001) between the irrigation and drought treatments (Table 2). At species level, only significant differences (P < 0.05) were found in the increase in diameter and number of branches. At provenance level, there were significant differences (P < 0.05) in the increase in height and diameter, root length and percentage of plants with secondary leaves. The interaction of moisture levels with species was not significant (P > 0.05) except in the percentage of secondary leaves. On the other hand, the treatment*provenance interaction had a significant effect (P < 0.001) only on the height and diameter variables.
Table 2 Significance values of the analysis of variance of the morphological variables of three provenances of Pinus cembroides and three of P. orizabensis at two moisture levels (drought and irrigation).
| Source of variation | Increase in height (cm) | Increase in diameter (mm) | Number of branches | Root length (cm) | Plants with secondary leaves (%) |
|---|---|---|---|---|---|
| Treatment | 0.0001 | 0.0001 | 0.0001 | 0.0001 | ns |
| Species | ns | 0.0001 | 0.0079 | ns | ns |
| Treatment*species | ns | ns | ns | ns | 0.0322 |
| Provenace (species) | 0.0001 | 0.0001 | ns | 0.0001 | 0.0435 |
| Treatment*provenance (species) | 0.0002 | 0.0001 | ns | ns | ns |
ns = not significant (P > 0.05)
Drought treatment negatively influenced plant growth; the variables increase in height, diameter, root length and total number of branches were lower by 20, 46, 30 and 31 %, respectively, compared to the normal irrigation control (Table 3). The increase in height was less affected, probably because a drought was applied in summer and autumn, which would affect the following year’s shoots but not those measured in 2018 (Dobbertin et al., 2010; Michelot, Brénda, Damesin, & Dufrêne, 2012).
Table 3 Growth variables of Pinus cembroides and P. orizabensis by moisture level (treatment).
| Treatment/ Species | Increase in height (cm) | Increase in diameter (mm) | Root length (cm) | Number of branches | Plants with secondary leaves (%) |
|---|---|---|---|---|---|
| Irrigation | 19.5 ± 0.55 a | 5.5 ± 0.07 a | 96.12 ± 1.81 a | 10.0 ± 0.3 a | 72.8 ± 2.6 a |
| Drought | 13.8 ± 0.55 b | 3.0 ± 0.07 b | 67.05 ± 1.81 b | 6.9 ± 0.3 b | 68.2 ± 2.6 a |
| Irrigation | |||||
| P. cembroides | 20.58 ± 0.73 a | 5.89 ± 0.11 a | 96.08 ± 2.49 a | 10.49 ± 0.48 a | 79.5 ± 3.7 a |
| P. orizabensis | 18.42 ± 0.73 b | 5.22 ± 0.11 b | 96.15 ± 2.49 a | 9.66 ± 0.48 a | 66.1 ± 3.7 b |
| Drought | |||||
| P. cembroides | 13.86 ± 0.73 a | 3.26 ± 0.11 a | 67.81 ± 2.49 a | 8.04 ± 0.48 a | 65.9 ± 3.7 a |
| P. orizabensis | 13.82 ± 0.73 a | 2.76 ± 0.11 b | 66.30 ± 2.49 a | 5.79 ± 0.48 b | 70.5 ± 3.7 a |
± standard error of the mean. Average values followed by different letters are different from each other (P = 0.05) by direct comparisons between pairs of means (PROC MIXED).
With respect to the irrigation plants, the variables increase in height and diameter, root length and number of branches of P. cembroides in drought were smaller by 33, 45, 30 and 23 %, respectively, while in P. orizabensis these same variables were smaller by 25, 47, 31 and 40 %, respectively (Table 3). Diameter growth was greater in P. cembroides in both treatments. This species had greater growth in irrigation, but also had a greater reduction in height due to drought effects than P. orizabensis, although in the latter, the negative effect on the number of branches was greater. These growth reductions occur due to the decline in photosynthesis (Matías & Jump, 2012).
Growth variables showed significant differences (P < 0.05) among provenances in each treatment (Table 4). The ones with the highest growth in irrigation and drought were from Santiago de Anaya (the one with the highest dryness of P. cembroides) and El Carmen (the one with the highest elevation of P. orizabensis). Likewise, the sources of greatest increase in diameter in irrigation were Santiago de Anaya and El Carmen, while in drought conditions it was Santiago de Anaya. Regarding root length, growth in drought was mainly limited in Colón (36 %), compared to irrigation, while Santiago de Anaya was the least affected provenance (22 %).
Table 4 Increase in height, diameter and root length of Pinus cembroides and P. orizabensis provenances in irrigation and drought.
| Species | Provenance | Increases | |||||
|---|---|---|---|---|---|---|---|
| Height (cm) | Diameter (mm) | Root length (cm) | |||||
| Irrigation | Drought | Irrigation | Drought | Irrigation | Drought | ||
| P. cembroides | Santiago de Anaya | 24.3 ± 1.3 a | 15.96 ± 1.26 a | 6.23 ± 0.19 a | 3.61 ± 0.19 a | 99.5 ± 3.1 a | 77.7 ± 3.1 a |
| Cadereyta | 20.7 ± 1.3 b | 13.31 ± 1.26 b | 5.78 ± 0.19 b | 2.96 ± 0.19 b | 95.8 ± 3.1 ab | 66.4 ± 3.1 bc | |
| Colón | 16.8 ± 1.3 c | 12.31 ± 1.26 b | 5.68 ± 0.19 b | 3.20 ± 0.19 b | 92.9 ± 3.1 b | 59.3 ± 3.1 d | |
| P. orizabensis | Tepeyahualco | 14.7 ± 1.3 c | 13.89 ± 1.26 ab | 4.70 ± 0.19 c | 2.47 ± 0.19 c | 92.4 ± 3.1 b | 65.0 ± 3.1 bc |
| El Carmen | 23.5 ± 1.3 a | 14.44 ± 1.26 ab | 6.16 ± 0.19 a | 3.06 ± 0.19 b | 100.1 ± 3.1 a | 70.6 ± 3.1 b | |
| Altzayanca | 17.1 ± 1.3 c | 13.14 ± 1.26 b | 4.80 ± 0.19 c | 2.74 ± 0.19 c | 95.9 ± 3.1 ab | 63.3 ± 3.1 c | |
± standard error of the mean. Average values followed by different letters are different from each other (P = 0.05) by direct comparisons between pairs of means (PROC MIXED).
The limitation of growth in these pinyon pines due to the effects of water deficit was foreseen as a result of what occurred in Larix decidua Mill., Pinus nigra J. F. Arnold and Pseudotsuga menziesii Mirb. var. menziesii (Eilmann & Rigling, 2012), which was attributed to stomatal closure and a hydraulic failure that affects carbon absorption and photosynthesis of plants (Ripullone, Guerrieri, Nole, Magnani, & Borguetti, 2007).
Response of biomass accumulation variables to water deficit
There were significant differences (P < 0.001) between treatments in all biomass variables and in the aerial dry weight/root dry weight ratio (Table 5). In the species*moisture level interaction, significant differences (P = 0.0019) were only found in the root biomass. In the moisture levels*provenance there was only significant interaction in the stem (P = 0.08) and root (P = 0.0253) biomass.
Table 5 Analysis of variance of the biomass and the aerial dry weight/root dry weight ratio of three provenances of Pinus cembroides and three of P. orizabensis under irrigation and drought treatments.
| Source of variation | Biomass | Aerial/root ratio | ||||
|---|---|---|---|---|---|---|
| Aerial | Stem | Needles | Branches | Root | ||
| Treatment | 0.0001 | 0.0002 | 0.0005 | 0.0001 | 0.0001 | 0.0001 |
| Species | 0.0488 | 0.0005 | ns | ns | 0.0001 | 0.0012 |
| Treatment*species | ns | ns | ns | ns | 0.0019 | ns |
| Provenance (species) | 0.0001 | 0.0009 | 0.0003 | 0.0055 | 0.0001 | 0.0002 |
| Treatment*provenance (species) | ns | 0.0800 | ns | ns | 0.0253 | ns |
ns = not significant.
The water stress imposed limited biomass in both species (Table 6). In P. cembroides, drought negatively affected aerial, stem, needle, branch and root biomass by 32, 44, 24, 27 and 51 %, respectively, while in P. orizabensis it was affected by 34, 42, 28, 41, and 49 %, respectively, compared to the data obtained in irrigation.
Table 6 Biomass variables by treatment of moisture levels (irrigation and drought) and by species (Pinus cembroides and P. orizabensis).
| Treatment/ Species | Biomass (g) | Aerial/root biomass | ||||
|---|---|---|---|---|---|---|
| Aerial | Stem | Needles | Branches | Root | ||
| Irrigation | 16.06 ± 0.37 a | 5.60 ± 0.22 a | 9.08 ± 0.24 a | 1.38 ± 0.05 a | 11.56 ± 0.39 a | 1.46 ± 0.04 b |
| Drought | 10.80 ± 0.37 b | 3.18 ± 0.22 b | 6.70 ± 0.24 b | 0.92 ± 0.05 b | 5.77 ± 0.39 b | 1.95 ± 0.04 a |
| Irrigation | ||||||
| P. cembroides | 16.43 ± 0.47 a | 6.02 ± 0.25 a | 9.06 ± 0.32 a | 1.34 ± 0.07 a | 12.89 ± 0.42 a | 1.32 ± 0.05 b |
| P. orizabensis | 15.70 ± 0.47 a | 5.18 ± 0.25 b | 9.09 ± 0.32 a | 1.42 ± 0.07 a | 10.23 ± 0.42 b | 1.60 ± 0.05 a |
| Drought | ||||||
| P. cembroides | 11.25 ± 0.47 a | 3.36 ± 0.25 a | 6.89 ± 0.32 a | 0.99 ± 0.07 a | 6.34 ± 0.42 a | 1.84 ± 0.05 b |
| P. orizabensis | 10.36 ± 0.47 a | 3.00 ± 0.25 a | 6.50 ± 0.32 a | 0.84 ± 0.07 b | 5.20 ± 0.42 b | 2.06 ± 0.05 a |
± standard error of the mean. Average values followed by different letters are different from each other (P = 0.05) by direct comparisons between pairs of means (PROC MIXED).
Water stress usually increases root biomass at the expense of aerial biomass; it has been speculated that this happens for the plant to access deeper water sources (Matías, González-Díaz, & Jump, 2014). The aerial biomass/root biomass ratio increased 34 % in the drought treatment; this same phenomenon was reported in an experiment with Pinus pinea L. (European pinyon pine, Villar et al., 2013), where the stem grew at the expense of the root. Although P. cembroides had a greater increase in this ratio (39 % vs. 29 %), this pine obtained a lower aerial/root biomass ratio and greater root biomass than P. orizabensis in both moisture treatments, which implies that P. cembroides has greater drought resistance.
The populations that showed greater biomass accumulation in stem, both in irrigation and in drought, were Cadereyta and Santiago de Anaya of P. cembroides (Table 7) and El Carmen of P. orizabensis (different by 19 % with P < 0.10), although they had a greater decrease in biomass than the rest of the provenances when under water deficit. Cadereyta and Santiago de Anaya were the provenances that accumulated the most root biomass, both in irrigation and in water deficit. Of the six tested provenances, Cadereyta is the one from the highest elevation and with the highest rainfall, while Santiago de Anaya has the lowest elevation and the highest temperature.
Table 7 Biomass characteristics of the provenances of Pinus cembroides and P. orizabensis subjected to irrigation and drought.
| Species | Provenance | Stem biomass | Root biomass | ||
|---|---|---|---|---|---|
| Irrigation | Drought | Irrigation | Drought | ||
| P. cembroides | Cadereyta | 6.65 ± 0.35 a | 3.63 ± 0.35 a | 14.34 ± 0.58 a | 6.60 ± 0.58 ab |
| Santiago de Anaya | 6.07 ± 0.35 a | 3.55 ± 0.35 ab | 13.82 ± 0.58 ab | 7.18 ± 0.58 a | |
| Colón | 5.34 ± 0.35 b | 2.89 ± 0.35 b | 10.51 ± 0.58 c | 5.25 ± 0.58 b | |
| P. orizabensis | El Carmen | 6.32 ± 0.35 a | 3.29 ± 0.35 ab | 12.67 ± 0.58 b | 5.84 ± 0.58 b |
| Altzayanca | 5.17 ± 0.35 b | 2.84 ± 0.35 b | 9.10 ± 0.58 d | 4.85 ± 0.58 b | |
| Tepeyahualco | 4.05 ± 0.35 c | 2.87 ± 0.35 b | 8.93 ± 0.58 d | 4.91 ± 0.58 b | |
± standard error of the mean. Average values followed by different letters are different from each other (P = 0.05) by direct comparisons between pairs of means (PROC MIXED).
P. cembroides had more root biomass, suggesting greater drought adaptation than P. orizabensis. On the other hand, P. cembroides had a decreased percentage of plants with secondary leaves as a result of going from normal to deficient irrigation; that is, it changed its development perhaps in order to save water. The accumulation of root biomass in the drought treatment of Santiago de Anaya of P. cembroides and El Carmen of P. orizabensis (19 % more) partially explains why the provenances of each species were more outstanding in the growth variables. Plants with a larger root system are more resistant to water stress (Simeonova & Hans, 2011). No association was found between the geographical location or any climatic variable with the performance of the provenances, except that the populations of warmer places (in general those of P. cembroides) had a greater stem base diameter. This variable showed positive correlations with the mean annual temperature (r = 0.78, P = 0.066) and the mean temperature of the coldest month (r = 0.82, P = 0.042) or the sum of days with temperatures >5 °C (r = 0.78, P = 0.067).
In order not to mix genotypes of these two allopatric species in their distribution areas, it is important to select the appropriate provenance if it is necessary to reforest limiting sites such as disturbed ones or a drier environment as has been predicted (Sáenz-Romero, 2011). Provenance selection is even more important if one considers that water deficit resistance differs between species (Eilmann & Rigling, 2012); for example, growth inhibition, as well as biomass, was lower than that reported in P. leiophylla Schiede ex Schltdl. & Cham. (Martínez et al., 2002), probably because the water stress imposed was relatively greater for this species, which inhabits less xeric places, than for the pinyon pines tested. In places that show water deficit it is important to select trees and provenances with attributes that grant resistance to drought and that can maintain higher growth rates than others that are susceptible to it. Moreover, trees under water stress conditions, by reducing their vigor (Allen, Breshears, & McDowell, 2015), are more susceptible to being attacked by pathogens and insects (Weed, Ayres, & Hicke, 2013); therefore, the selection of species, provenances and individuals that better evade or tolerate drought, without loss of growth, will be a priority in a water stress scenario.
Conclusions
The 27-month-old plants of Pinus cembroides showed greater growth and drought resistance than those of P. orizabensis; in addition, they had higher growth in normal moisture conditions. There are differences among provenances within each species in restrictive and non-limited moisture conditions. In water deficit, populations from warmer places, mainly P. cembroides, had larger-diameter stems. The provenances that had less stem and root biomass in moisture had less biomass loss, indicating evasion mechanisms when under drought conditions. The establishment of reforestation by mixing the two species or their provenances will affect adaptation and therefore their productivity.
