Study area

The study was carried out in commercial E. urophylla plantations established in the municipality of Huimanguillo, Tabasco, Mexico (17° 55’ N, 94° 06’ W, at 30 m average altitude) (Figure 1). The climate is hot and humid (annual average), with copious summer rains, 2500 mm mean annual precipitation, and 26 °C mean annual temperature. The plantations are grown in Phaeozem soil type ( ^{INEGI, 2005}).

Figure 1 Geographical location of commercial Eucalyptus urophylla forest plantations established in Huimanguillo, Tabasco, Mexico. 

Plantations characterization

The study was carried out in 1-7 years plantations. The space between plants and rows is 2×3 or 2.5×3.5 m, with an average density of 1667 and 1143 trees per hectare. The plants are improved E. urophylla clones (Table 1) and their purpose is to supply the domestic pulp market.

Table 1 Dasometric values of Eucalyptus urophylla’s CFPs (initial and final measurements). 

Dn: Diameter at breast height (cm), At: total height (m), DE: standard deviation, Min: minimum, Max: maximum, †: Plantation harvested during the study.

Filed data collection

Above-ground net primary productivity (ANPP)

The ANPP calculation in Mg ha^-1 year^-1 included the integration of the increment in organic matter and the production of litterfall, over a given time interval (^{Clark et al., 2001b}; ^{Hanson et al., 2003}; ^{Kotowska et al., 2015}).

ANPP was estimated using the method described by ^{Clark et al. (2001a}), which considers the total biomass increment, the individuals’ mortality, the joint growth of evaluated trees, and the litterfall production in the ecosystem, assuming a continuous replacement rate, as represented by the following expression:

The individual biomass was estimated using the allometric equations developed by Hernández-Ramos et al. (unpublished results) for E. urophylla in the study area (Table 2). The values of Diameter at breast height (Dn) and total height (At) of the trees measured in July 2014 and August 2015, at 28 sampling sites, were used for these equations.

Table 2 Allometric equations used to estimate the total and per components above-ground biomass of Eucalyptus urophylla, in Huimanguillo, Tabasco, Mexico. 

Dn: Diameter at breast height (1.30 m) (cm), At: total height (m).

Biomass increment (Mg ha^-1 year^-1): total and by structural component biomass (trunk, branches, and leaves) was estimated at the beginning (t₁) and at the end (t₂) of the analysis period. Biomass of the trees lost by mortality was added to the second sampling. The increase is defined as the difference in biomass between t₂ and t₁, according to the following equation (^{Klepac, 1983}; ^{Clark et al., 2001a}):

where: Bt_t2't1: total above-ground biomass calculated in time 1 and 2 (Mg ha^-1 year^-1).BΘ: biomass of trees lost by mortality (Mg ha^-1 year^-1).

Annual fine litterfall: it was estimated adding the total litterfall (g m^-2 month^-1) that fall monthly per component in 1 m², during 12 months, in order to complete one E. urophylla growth cycle in plantation conditions.

Comparative analysis of ANPP and litterfall production

Each sampling site was considered as a completely randomized distribution experimental unit. Each site’s age was considered as the primary factor (treatment), the month was the secondary factor, and the litterfall production was the dependent variable. Means of total and per component ANPP litterfall production were analyzed with ANOVA. The comparative test included the monthly and annual results, in order to determine the higher and lower production season. The production differences between plantations were analyzed using Tukey’s multiple comparison test. Statistical analyzes were performed in SAS 9.4 statistical software.

Litterfall production rate by structural component and total

There was a great variation in the annual total litterfall production (TLP) between different age plantations. The annual total litterfall production estimated ranged from 4.068 to 5.628 Mg m^-2 year^-1 for 1-7 years plantations. The largest production was observed in the 7-years plantation, followed by the 2-years plantation, and the smaller values belonged to the 4- and 5-years plantations. The remaining plantations had similar TLP values (Figure 2).

Figure 2 Annual total litterfall production, leaves, branches (A) and fruits (B), in Eucalyptus urophylla plantations, in Huimanguillo, Tabasco, Mexico. 

The annual total and per component litterfall productions were statistically different (p=0.05) between ages (Table 3). Litterfall low values in 4- and 5-years plantations can be attributed to a greater competition with the understory, generated by the stoppage of weed control practices, given the species’ dominance at that age, and by the clonal differences between plantations.

Table 3 Total and by structural component average annual litterfall production (g m^-2 year^-1) in Eucalyptus urophylla plantations, in Huimanguillo, Tabasco, Mexico. 

PTH: annual total litterfall production. Means with a different letter in each column are statistically different; µ: PTH proportion mean for each component.

The production trends per component (leaves, branches and fruits) were similar to those of the overall production. The largest number of fallen leaves was found in the 7-years plantation and the lowest in the 4- and 5-years plantations. The branches maximum value was presented in the 3-years plantations and the minimum in the 1-years plantations. The highest fruit production occurred in the 6- and 7-years plantations.

Leaves made the greatest contribution to litterfall, representing 91.62 to 67.02 % in 1 to 7 years plantations. The second largest contribution was made by branches, with a minimum and maximum of 6.5 and 26.80 %, respectively. Fruits represented less than 10 % of TLP (Table 4).

Table 4 Average monthly litterfall production (g m^-2 month^-1) in Eucalyptus urophylla plantations, in Huimanguillo, Tabasco, Mexico. 

PTH: total litterfall production. Means with a different letter in each column are statistically different.

The average annual litterfall production (4.289 Mg ha^-1 year^-1) was similar to the production in commercial plantations of temperate climate species, such as 13 and 15 years P. patula plantations without fertilization (5.768 and 4.365 Mg ha^-1 year^-1) in the north of the State of Veracruz (^{Vásquez et al., 2015}); 26-years-old P. radiata, with the vegetation associated with 3.206 Mg ha^-1 year^-1, in the Valdivia region, Chile (^{Huber and Oyarzún, 1983}). ^{Gutiérrez et al. (2012}) reported lower litterfall production values in P. greggii and P. cembroides plantations established in Coahuila, Mexico (1.072 and 0.976 Mg ha^-1 year^-1), which is understandable because P. greggii and P. cembroides are slow growing species, compared to E. urophylla.

In species established in tropical regions (specifically in Junin, Peru), ^{Gamarra (2001}) reported that E. globulus Labill, produced 4.99 Mg ha^-1 year^-1 of litterfall. Compared to plantations in temperate regions, plantations in tropical climates show higher production at a younger age. This is attributed to the fact that tropical regions are more productive than temperate ones, due to the high water availability and higher temperatures, which are variables that significantly influence the tropical species’ growth; the opposite occurs in temperate ecosystems (^{Gómez and Gallopin, 1991}).

Monthly litterfall production rate

The months with the highest production of leaves and branches -regardless of plantation age-, were April, May and June. Joint production during these months matched 37.9 % of the annual total production. The highest fruit production was recorded in February and March, mainly in over 5-years plantations (Figure 3).

Figure 3 Total and per component monthly litterfall: leaves, branches (A), and fruits (B), in Eucalyptus urophylla plantations in Huimanguillo, Tabasco, Mexico. 

The monthly litterfall production was statistically different from month to month (p=0.0001). Thus, it was possible to differentiate the trees’ litterfall during the year, regardless of plantation age (Table 5). The largest production occurred during April, May, June, and October: the first three months match the end of the dry season, so litterfall is attributed to the plants’ water stress and the generation of new leaves. The greater litterfall accumulation in October could be the result of the season’s strong winds or the torrential rains.

Table 5 Above-ground biomass (Mg ha^-1) and percentage per initial and final biomass component accumulated per plantation age for Eucalyptus urophylla in Huimanguillo, Tabasco, Mexico. 

E_1-2, E_2-3, E_3-4, E_4-5, E_5-6, E_6-7: Plantation age at the beginning and end of the measurement; Bf: trunk biomass, Bh: leaf biomass, Br: branch biomass; %: percentage based on total biomass (Bt).

The behavior of the maximum production of each component, leaves and branches, was similar to TLP. The branches values were lower from July to September. The fruit fall was higher during October, February and March, with statistically higher values in older plantations, where the trees have a greater phenological maturation (Figure 3B).

^{Castañeda-Mendoza et al. (2012}) asserted that the maximum litterfall in Bambusa aldhamii plantations, in Huatusco, Veracruz, Mexico, occurs from February to July, ^{Gutiérrez et al. (2012}) reported that the most important contributions of P. greggii and P. cembroides litterfall in plantations in Coahuila, Mexico, occurred during May and June. ^{Di Stefano and Fournier (2005}) concluded that the greatest litterfall in monoculture plantations of tropical species occurs during the dry season and during the strong winds period.

In the study site, there is less precipitation and higher temperature from February to June, which causes water stress in plants and leaf loss. Our results are similar to those obtained in natural pine-holm oak forests, with a larger production from March to May; additionally, during October and November, they presented a slightly higher accumulation, which was attributed to meteorological phenomena effects (^{Rocha and Ramírez, 2009}).

Estimation of above-ground biomass

The trunk biomass proportion (Bf) in relation to Bt was higher in older trees (Table 6), due to biomass accumulation in its support structure; this is typical of young fast-growing plantations (^{Reed and Tomé, 1998}). In contrast, the leaf (Bh) and branches (Br) biomass proportion decreased in older plantations. However, the production of these components was relatively constant across all ages; meanwhile, the productive capacity of the site affects this characteristic. In the initial and final measurements, the biomass average proportion per component was 85.8, 4.0, and 10.3%, for Bf, Bh, and Br respectively. At 7 years, the total biomass accumulated by E. urophylla was 148.0 Mg ha^-1. The annual increment of the evaluation period represented 33.32, 25.55, 11.77, 14.31, 16.87, and 21.54 Mg ha^-1 year^-1 in the six plantations (Table 6) and an annual general average of 20.56 Mg ha^-1 year^-1. ^{Binkley and Ryan (1998}) reported similar values for total biomass (323 Mg ha^-1) in 16-years E. saligna plantations; the average annual increment would be 20.3 Mg ha^-1 year^-1. ^{Geldres et al. (2006}) reported accumulated biomass values of 73.1, 111.8, and 159.5 Mg ha^-1 in 4-, 5-, and 6- years E. nitens plantations, and annual biomass increments of 39.2 Mg ha^-1 in 4 and 5 years plantations, and 50.1 Mg ha^-1 in 5 and 6 years plantations. These estimates are higher to those of the present study. E. nitens’ high values are associated with weed control and fertilization during the first three years and thinning at five years (which matches the stage at which trees grow more). In contrast, in this study plantation management did not match any specific development stage.

Table 6 Above-ground net primary productivity (Mg ha^-1 year^-1) total and per component for Eucalyptus urophylla plantations in Huimanguillo, Tabasco, Mexico. 

E_1-2, E_2-3, E_3-4, E_4-5, E_5-6, E_6-7: Plantation age at the beginning and at the end. Means with different letters in each row are statistically different.

Estimation of above-ground net primary productivity

The estimated average ANPP was 26.26 Mg ha^-1 year^-1, 84.0 % was the result of the increment in living biomass and 16.0 % to the increment in the biomass incorporated into the soil as fine litterfall. The average contribution to ANPP was: 20.23 Mg ha^-1 year^-1 (77.0 %) to Bf; 3.62 Mg ha^-1 year^-1 (13.8 %) to Bl; and 2.39 Mg ha^-1 year^-1 (9.1 %) to Br, for all ages (Figure 4). The variance analysis indicated significant differences (α=0.0001) in ANPP by plantation age (Table 5). The distribution of the ANPP data set at each age is variable, thus differences in their means are indicated.

Figure 4 Eucalyptus urophylla’s above-ground net primary productivity (ANPP) and: (A) contribution of trunk biomass (Bf), (B) leaf biomass (Bh), (C) branch biomass (Br), (D) average. Tabasco, Mexico. 

The variability in ANPP with different ages was confirmed with the comparison of means, which indicated that the highest productivity of plantations was observed in the first years of growth, when the trees increase in size and their nutrient assimilation is more efficient. The ages with the highest ANPP increment were 1-2 and 2-3 years, with 37.33 and 30.37 Mg ha^-1 year^-1 values. A high value was observed during the 6-7 year, with 26.28 Mg ha^-1 year^-1, indicating that the ANPP declines slightly with age. Meanwhile, the low scores in the 3-4, 4-5, and 5-6 years may be due to the soil productive capacity, the competition for space and nutrients with herbaceous plants, the lack of fertilization or unrecorded differences between clones, and to the initial stage of the production of reproductive organs.

Young plantations presented the highest above-ground net primary productivity, which matches the observations of ^{Tuner et al. (2009}) and ^{Ernst et al. (2000}), who indicated that the growth rate is greater at a younger age and, consequently, an increase in carbon capture. ^{Binkley and Ryan (1998}) recorded the following ANPP in E. saligna plantations: 27.9 Mg ha^-1 year^-1 from 2 to 4 years, 22.4 Mg ha^-1 year^-1 at 6 years, and 10.9 Mg ha^-1 year^-1 at 10 and 16 years. Thus, the productivity pattern decreased as the plantation age increased. ^{Ares and Fownes (2000}) determined 15.8 and 23.8 Mg ha^-1 year^-1 ANPP in 28 to 36 years E. saligna plantations; these estimates were low due to age; also, ANPP decreased with altitude and in areas with low precipitation.

According to ^{Ignacio et al. (2005}), as the E. urophylla plantation grows older, the growth and yield of trees decreases, as a result of the competition for space or the change in the species’ phenological stage; besides, they indicated that diameter and volume growth become stable at 3 years, and productivity also decreases. The ANPP average value in our study (26.26 Mg ha^-1 year^-1) was higher than the value recorded for tropical ecosystems (21.60 Mg ha^-1 year^-1) (^{Murphy, 1975}), which shows that the E. urophylla plantations analyzed present high biomass productivity.