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Article

Biomass Losses Caused by Teratosphaeria Leaf Disease in Eucalyptus globulus Short Rotation Forestry

by
Severiano Pérez
*,
Carlos J. Renedo
,
Alfredo Ortiz
,
Félix Ortiz
and
Agustín Santisteban
Department of Electric and Energy Engineering, University of Cantabria, 39005 Santander, Spain
*
Author to whom correspondence should be addressed.
Forests 2017, 8(11), 447; https://doi.org/10.3390/f8110447
Submission received: 19 September 2017 / Revised: 9 November 2017 / Accepted: 14 November 2017 / Published: 17 November 2017
(This article belongs to the Section Forest Ecophysiology and Biology)
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Abstract

:
This article presents the results of a study that examines the loss of biomass and energy, per hectare, caused by Teratosphaeria leaf disease (TLD) in Eucalyptus globulus short rotation forestry. The 95 Eucalyptus globulus taxa analyzed are from seeds of open pollinated families of both Spanish and Australian origin. Tree height and diameter were measured and the crown damage index (CDI) assessed at 27 months of age. Taxa that have a certain tolerance to the disease have been identified. The taxon identified as code 283 is the one that shows lower CDI (42%) and with an average volume that exceeded 0.017 m3 at 27 months of age. Biomass losses were determined for each fraction of dry biomass of the tree (leaves, branches, twigs and bark) based on CDI. These losses were translated into terms of energy lost per hectare, depending on the CDI. A comparison was then carried out between the productivity of Eucalyptus globulus exhibiting various levels of TLD severity and poplar and willow clones used for bioenergy in Europe. In our region, the results show that despite the losses of biomass associated with TLD, Eucalyptus globulus remains competitive as long as CDI values are lower than 56%.

Graphical Abstract

1. Introduction

The replacement of fossil fuels by bio-based energy sources contributes to a more sustainable world [1]. Spain is a country with huge foreign energy dependence, however, it has a great deal of potential energy that could be derived from renewable resources. For the particular case of Cantabria in northern Spain, forest based biomass has a promising future since adequate soil and climatic characteristics are present. The region has an extensive non-exploited forest area which may be used for new plantings with energy purposes.
Biomass is the third largest source of energy in the world [2]. In addition to abundance, biomass offers great versatility when being used as primary energy for the generation of electricity, heat or fuel for transportation [3]. One way to generate biomass is through short rotation forestry (SRF). These are characterized by fast growing species used in planting densities ranging from 1000 to 20,000 stools ha−1 in poor soils and reduced short tree shifts. Some examples are species belonging to the genera Populus, Eucalyptus, Pinus, Acacia and Salix [4,5,6,7,8,9,10,11,12,13]. Most research today involves the genera Populus and Salix, commonly known as poplar and willow. In fact, clones of these genera have been specifically selected for biomass generation in short rotations [14,15,16,17,18,19]. Research has focussed on these genera due to interest of countries of northern Europe and America where the amount of water that these species require during the vegetative stage occurs naturally.
The genus Eucalyptus performs exceedingly well as an energy crop in temperate forests, such as those of northern Spain, where water availability is a limiting factor for the growth of poplar and willow during the spring and summer [10,11,20]. The appropriateness of this genus is justified from the production and the energy point of view, since it combines high density biomass [21] and good calorific values [22,23]. At present, the superiority of the genus Eucalypus to generate biomass in SRF is limited by the appearance of a biotic agent that produces the disease known as Theratosphaeria Leaf Disease (TLD), especially in the Eucalyptus globulus. The genus Eucalyptus can suffer from a large number of fungal leaf diseases, however TLD is seen as the most serious [24,25,26,27]. A single Theratosphaeria species, Theratosphaeria nubilosa, is responsible for the bulk of the damage to Eucalyptus trees in Spain. Infection of leaves occurs when acospores germinating on the leaf surface produce germtubes which enter the leaf via stomata [28]. The most intense attack occurs during the months of late summer and early autumn, while a recovery of the tree normally occurs in springtime. There are many studies in the scientific literature that examine the impact and control of diseases on forest trees that generate energy in short cycles [29,30,31,32,33]. These studies, mainly based on the genera poplar and willow, examine ways to manage diseases by the use of chemicals or by selection of genotypes tolerant to pests and diseases.
Harvest age ranges from two to four years. Eucalyptus species are characterized by two types of foliage over their lifetime: juvenile and adult foliage. TLD affects juvenile foliage causing extensive defoliations and a marked growth reduction, which, in combination with frost, can kill the tree [28,34,35,36,37,38,39]. It is worth highlighting that the juvenile stage of the species is of greatest interest for energy crops, because of short tree shifts. This article is the result of a research project that began in 2006 with the establishment of a trial with genetic material from Eucalyptus globulus stands of Australian and northern Spanish origin. Each family is identified by a code. The goal was to compare the losses of biomass and energy, per hectare, versus the degree of importance of the disease. This will allow the productivity of this genus to be evaluated respect to other species used in SRF. The experimental results enabled us to identify those codes showing some tolerance to TLD. At 27 months of age, for each code, the heights and diameters of the trees have been measured, obtaining the corresponding volume. At this time, the crown damage index was defined and evaluated and also assessed. The biomass loss as a function of CDI was then determined for each fraction that forms the tree (leaves, branches, twigs and bark), and the total loss of biomass per hectare. Productivity (t ha−1) and energy losses (Megajoules ha−1) have been calculated based on the CDI. This allows the calculation of CDI levels below which the cultivation of Eucalyptus globulus can be viable and/or comparable with clones of poplar and willow used in short rotation coppice. This can be a first step in obtaining tolerant genetic material that can be used to generate biomass in areas with prevalence of TLD.

2. Materials and Methods

In March and April 2006, a E. globulus short rotation stand was established in Cantabria (northern Spain), latitude 43°28′ N, longitude 3°48′ W at 120 meters above sea level. This period is very suitable for the development of this species and TLD appears to be the single most limiting biotic agent. The site is characterised by a climate with moderate temperature variation and regular rainfall. Long-term values for mean air temperature and annual rainfall are 13.8 °C and 598 mm respectively. The stand consists of 2375 trees belonging to taxa from two sources: Australian (50 taxa), supplied by CSIRO Forestry, and Spanish (45 taxa), obtained from seeds of trees from forests in northern Spain. Both sources are from open-pollinated families. The trial contained 25 replicates with 95 individuals per replicate. Each replicate contained one individual (code) arranged at random. The stand frame used was 2.5 × 2.5 m which corresponds to 1600 plants per ha.
At the time of planting, the soil was fertilized with 20–30 g per plant of a controlled release fertilizer 11-22-9 (NPK) + 6 MgO. At the age of one year, the soil was again fertilized with 300 g per plant of complex fertilizer 15-15-15 (NPK).
At 27 months of age, for each tree, one branch was taken randomly at breast height. Once each branch was cut, they were then transported to the laboratory in a sealed polyethylene bag. Simultaneously, the degree of defoliation (D, %) due to the disease was evaluated in the field using the diagrams given by [39,40] for this purpose. Once in the laboratory, the samples were evaluated for severity (S, %), defined as the percentage of leaf area affected [39,40]. Taking into account the severity and the defoliation, the overall rate of damage Crown Damage Index, (CDI, %) is defined by the expression (1) encompassing both variables [41]. Obviously, the severity affects only the leaves that have not yet fallen.
CDI = D + S ( 100 − D ) 100
Height (H, m) and diameter (D, m) was measured using a laser hypsometer Vertex and a mechanical calliper respectively. In order to calculate the volume (V, m3) with bark, the formula given by [42] based on the total height and diameter at breast height over bark (DBHOB), was followed. From the volumes, the amount of biomass lost as a function of CDI due to TLD was determined. For this, the weight of dry biomass of each fraction “i” (Wi, kg) was first calculated for each code, using the expression (2) [43] and the parameters in Table 1. The amount of biomass lost was obtained by means of the difference between the CDI zero (obtained by regression) and the CDI evaluated for each code.
W i = exp ( α + β ln D + γ ln H )
From the amount of biomass calculated, the loss has been estimated for each CDI.
In order to determine the amount of energy loss, the gross and the net calorific values (GCV and NCV) of Eucalyptus globulus in the juvenile stage have been obtained using the method proposed by [44] in a calorimeter. The characteristics of the apparatus and the methodology used are described in [23].
The average NCV of the fractions (dry biomass) that make up the biomass of Eucalyptus globulus at juvenile age, and that were studied in the laboratory [23]. For the calculation of the weighted average value of NCV, the weight percentage of each fraction of the tree, given by [45], has been taken into account. These percentages are related to Cantabria since they were determined in juvenile stands of north western Spain. Studies carried out elsewhere [46] show that the weight percentages of tree fractions vary with age and diameter, however, this effect is neglectable in SRF.
Data analyses were performed using the Statistical package SPSS (PASW) 18.0 (SPSS Inc., Chicago, IL, USA), comparing CDI means and tree volume for the different codes analyzed.
The experimental results enabled us to identify those codes showing some tolerance to MLD. At 27 months of age, for each code, the heights and diameters of the trees have been measured, obtaining the corresponding volume. At this time, the Crown Damage Index (CDI) was defined, evaluated and also assessed. The biomass loss as a function of CDI was then determined for each fraction that forms the tree (leaves, branches, twigs and bark), and the total loss of biomass per hectare. Productivity (t ha−1) and energy losses (MJ ha−1) have been calculated based on the CDI. This allows the calculation of CDI levels below which the cultivation of Eucalyptus globulus can be viable and/or comparable with clones of poplar and willow used in short rotation coppice. This can be a first step in obtaining tolerant genetic material that can be used to generate biomass in areas with prevalence of MLD.

3. Results and Discussion

Table 2 shows the results of the measurements in the stands. Heights and diameters are related to the CDI at the age of 27 months. The first column gives the origin identification code. ANOVA revealed significative differences in the CDI mean values for the different codes (p-value = 0.05). The average value of CDI is 60.64%, however, the codes 283, 105, 255, 102 and 341 present severities below the average, with values of 42.67, 49.03, 51.09, 52.09, 52.40% respectively. This study shows that there are some codes less sensitive to TLD than others. In the scientific literature, this variation in the resistance to the disease is associated to genetic factors and not environmental ones [27,38,47,48]; this way, tolerant plants show this property everywhere.
There are significative differences between the average volumes achieved at 27 months by each code (p-value = 0.001). The codes previously mentioned achieved an average volume of 17.13 × 10−3, 14.99 × 10−3, 10.96 × 10−3, 10.82 × 10−3 and 11.04 × 10−3 m3, respectively, which can be compared with the average value of 9.20 × 10−3 m3. There is also a significative negative correlation (r = −0.638; p < 0.0001) between the individual average volume at 27 months and the CDI. This means that those codes showing lower sensitivity to TLD are the most suitable for the biomass generation. In experimental stands with no damage from TLD established in previous years, average volumes of only 9.7 × 10−3 m3 per tree were obtained at 49 months of age without fertilisation. The high volumes we obtained in this study are due to the fertilization provided in conjunction with the soil quality in the stands on which this study is based. These two factors enable a swift recovery from the attack of TLD and permit the subsequent development of the tree during the second spring, allowing the change from youth to adult leaf at a younger age. As a result, these data cannot be compared with those of other stands with different bioclimatic features and fertilizations. However, one can compare the effects of TLD among the various families included in this study and provide an estimate of the biomass loss in terms of TLD damage.
Figure 1 shows the weight percentage of leaf loss over a null CDI. It is worth noting that as the CDI increases the leaf loss is more pronounced, reaching values close to 48% for CDI above 60%. In more specific terms, at 27 months, the average loss of leaves per tree is approximately 1.5 kg. This loss not only results in a reduction of biomass and of tree growth, but also can favour the development of other pathogens due to the weakness of the tree after the first attack of TLD, and could possibly lead to the tree’s death [49].
Similarly, Figure 2 shows the loss percentage of wood with bark. It can be observed that the loss of this fraction at a CDI of 60% is between 50% and 60% in weight. Thus, for juvenile Eucalyptus globulus with 60% CDI, the average losses of dry wood and bark per tree are about 3 kg.
Regarding the branches and twigs fraction, Figure 3 shows the results of the losses depending on the CDI value. For a 60% CDI, the average loss percentage reaches 50%, compared to a CDI of zero. This implies a loss per tree of around 1.25 kg of branches and twigs for this species, at 27 months of age.
Comparing Figure 1, Figure 2 and Figure 3, it can be seen that losses increase with increasing CDI, and that wide differences appear between codes. For example, code 241 incurs lower losses than other codes with a similar CDI, and it exhibits comparable losses to other codes with lower CDI levels. For a given CDI, the disease causes greater loss percentages in wood and bark than in the other fractions that comprise the tree. Figure 4 brings together all the biomass (leaves + branches + twigs + bark) representing the weight in kg of dry biomass per tree, depending on the CDI. For a CDI of around 42%, the dry biomass production at the age of 27 months is more than 8 kg per tree, whereas for CDI higher than 66%, the dry biomass production is lower than 3.8 kg per tree. These results show a 200% difference in production when the CDI varies by only 20%. This fact suggests a possible method of selection for the future, based on the observation that distinct families or individuals present a certain tolerance to TLD. They could be the genetic basis of viable energy stands of Eucalyptus globulus in the future. In our case, the codes 105 and 283 are those that generate more biomass in areas with high prevalence of TLD, manifesting a certain tolerance to the disease.
Considering the data in [23] and the biomass losses, the amount of energy lost (MJ ha−1) in a juvenile stage Eucalyptus globulus stand, based on the CDI, has been estimated (see Figure 5). A planting density of 1600 stems ha−1 and a rate (number of trees that mortalyted 12 months of age) of 10%, were taken into account. This death rate can be considered as an extensively managed plantation representative of an E. globulus stand that has not been damaged by external agents. The results shown in Figure 5 relate biomass losses with energy losses. In our case, it is observed that between CDImaximum and CDIminimum the losses range between 83,000 and 184,000 MJ ha−1 respectively.
Figure 6 compares the E. globulus dry biomass yields, in Megagrams ha−1, from our study, with yields from other genera used as SRF (poplar and willow clones) in northern Europe.
According to [8,50], poplar and willow clone production, in experimental stands with densities of 16,600 stems ha−1, varies between 10 and 40 Mg ha−1 and 15 and 38 Mg ha−1, respectively, at five years of age and depending on fertilization treatments and soil characteristics. This implies an annual average yield of 6 and 4 Mg ha−1 for poplar and willow, respectively. It is worth highlighting that two codes of Eucalyptus globulus, even with much lower planting densities (see Figure 6), can achieve annual productions exceeding those of poplar and willow clones. It can be concluded that these two codes, namely 283 and 105, are most suitable for bioenergy stands in areas with high TLD prevalence.
It should be noted that average productions of poplar and willow clones are calculated for five year rotations and planting densities 10 times higher than those in this study. Moreover, in this study, the analysis was performed on trees at the age of 27 months. This fact has relevance since the damage caused by TLD in Eucalyptus globulus occurs mainly from the second year on, specifically between 22 and 30 months of age [50]. Thus, if the rotation period is less than two years, the damage caused by TLD would be lower, and productivity per hectare would increase. This option would entail much higher planting densities, difficulty with regrowth, soil depletion due to overexploitation; in a word, significantly greater environmental impact. In practice, this strategy, from a purely business standpoint, would involve costs not feasible today. However, it would be interesting to test different rotation periods and planting densities in order to optimize production of this tree species in areas with TLD prevalence.
In the stands of poplar and willow clones, planting densities are around 16,600 stems ha−1, [8] which represents a significant increase in the planting and fertilization costs compared to those of Eucalyptus globulus. From an economic standpoint, this fact favours Eucalyptus globulus, since, with planting densities several times lower than poplar and willow, this species can attain similar biomass productivities, even when TLD is present. Despite the impact of the TLD on the plantations of Eucalyptus globulus, this previously selected species can be used as SRF in temperate places where the fungus is a limiting factor during the spring and summer months. Knowledge about the control of the disease [51] together with the selection of individuals will allow the establishment of viable E. globulus plantations.

4. Conclusions

The attack on Eucalyptus globulus short rotation stands by the foliar disease TLD significantly reduces its productivity, since it is precisely the juvenile stage that is affected. There are taxa (identified by codes in this study) of E. globulus in which the disease severity is significantly lower than the average, suggesting that these families are endowed with a certain tolerance to the disease, as compared to their counterparts.
The loss of dry biomass varies according to the CDI. For trees at 27 months of age, with a CDI of around 60%, the loss ranges between 8 and 10 Mg ha−1. This total loss corresponds to the sum of the partial losses that make up the biomass. The greatest losses are seen in the fraction representing wood and bark, which, at 60% CDI, experiences a reduction of approximately 70% in weight.
The weighted average NCV of juvenile E. globulus, (dry biomass), is 16,774 kJ kg−1. In this study, when combined with the loss of biomass per ha, the energy loss per area unit range between 83,000 and 184,000 MJ ha−1. This loss could be translated into economic terms by considering the current high prices for electricity obtained from forest energy crops.
Despite the incidence of TLD in stands of E. globulus, their productivity is similar (when CDI values are low enough), to other species used for energy purposes (clones of poplar and willow), and this happens even when the planting densities of the E. globulus stands are much lower. In general, E. globulus biomass yields can be considered similar to those of poplar and willow when the CDI is lower than 56%. This finding suggests a future research focus which could involve the selection of families tolerant to the disease that would serve as the genetic basis for future stands. In our case, the families represented by codes 283 and 105 are best suited for this purpose.
The presence of the foliar disease TLD in stands of E. globulus influences the forestry and management of such plantations. An effective response to the threat posed involves the selection of individuals and families tolerant to disease. One barrier to overcome is the known difficulty of E. globulus to be cloned by cuttings due to low rooting capacity. This limitation, as well as the tolerance to TLD appears to be strongly linked to the genetics of each individual and/or family.

Acknowledgments

The authors wish to thank the Council on Research and Technological Development of the University of Cantabria and the company Sniace, S.A. for its great help.

Author Contributions

For research articles with several authors, a short paragraph specifying their individual contributions must be provided. The following statements should be used “S. Pérez conceived and designed the experiments; C.J. Renedo, performed the experiments; A. Ortiz and F. Ortiz analyzed the data; A. Santisteban contributed reagents/materials/analysis tools; S. Pérez, wrote the paper.” Authorship must be limited to those who have contributed substantially to the work reported.

Conflicts of Interest

The authors declare no conflict of interest.

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Forests 08 00447 g001 550
Figure 1. Leaves losses at 27 months of age according to the CDI.
Figure 1. Leaves losses at 27 months of age according to the CDI.
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Forests 08 00447 g002 550
Figure 2. Wood with bark loss at 27 months of age according to the CDI.
Figure 2. Wood with bark loss at 27 months of age according to the CDI.
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Forests 08 00447 g003 550
Figure 3. Branch and twig loss percentage at 27 months of age, according to the CDI.
Figure 3. Branch and twig loss percentage at 27 months of age, according to the CDI.
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Forests 08 00447 g004 550
Figure 4. Total weight of dry biomass per tree depending on the CDI (age 27 months).
Figure 4. Total weight of dry biomass per tree depending on the CDI (age 27 months).
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Forests 08 00447 g005 550
Figure 5. Dry biomass and energy losses per ha, at 27 months of age, according to the CDI.
Figure 5. Dry biomass and energy losses per ha, at 27 months of age, according to the CDI.
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Forests 08 00447 g006 550
Figure 6. Eucalyptus globulus annual productivity (Mg ha−1) versus Poplar and Willow clones.
Figure 6. Eucalyptus globulus annual productivity (Mg ha−1) versus Poplar and Willow clones.
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Table
Table 1. Regression coefficients for Eucalyptus globulus stands [43].
Table 1. Regression coefficients for Eucalyptus globulus stands [43].
Fractionαβγ
Total biomass−2.89820.19841.7425
Leaves0.78970.29210.8769
Wood + bark−6.85790.24742.2294
Rest−2.56690.33461.3349
Table
Table 2. Mean, standard deviation (Std Dev) and standard error mean (Std Err Mean) of heights (H), diameters (D), volumes (V × 10−3) and CDI for all codes of Eucalyptus globulus at 27 months of age.
Table 2. Mean, standard deviation (Std Dev) and standard error mean (Std Err Mean) of heights (H), diameters (D), volumes (V × 10−3) and CDI for all codes of Eucalyptus globulus at 27 months of age.
CodeH (m)Std DevStd Err MeanD × 102 (m)Std DevStd Err MeanV × 103 (m3)Std DevStd Err MeanCDI (%)Std DevStd Err Mean
324.221.060.2493.341.070.2526.322.690.63567.057.421.749
655.191.140.2384.331.310.2729.654.440.92656.2615.463.225
684.931.310.2723.971.360.2848.603.960.82664.888.661.806
864.641.340.2923.761.480.3237.974.500.98159.7214.303.121
894.611.040.2163.741.060.2207.472.920.60962.916.651.387
905.071.250.2724.101.260.2748.943.810.83166.308.181.785
924.881.080.2213.881.020.2078.032.950.60263.778.301.694
964.720.950.2033.820.960.2057.682.990.63762.298.641.842
1014.800.920.1963.871.150.2468.003.520.75163.905.901.257
1025.031.580.3724.651.640.39710.825.931.43952.0919.654.632
1045.610.970.2064.891.180.25111.444.020.85657.3312.872.744
1056.001.270.2595.651.800.36714.997.681.56849.0317.983.670
1525.051.960.4084.761.630.35511.475.711.24560.759.972.125
2134.021.240.3583.041.060.3055.702.830.81668.408.282.391
2164.760.990.1973.890.930.1877.842.810.56162.607.311.462
2235.381.320.2694.441.470.30110.405.731.17063.335.421.107
2255.650.890.1824.680.930.18910.783.450.70461.838.711.779
2324.891.190.2394.061.160.2328.553.690.73863.507.491.497
2355.230.870.1864.360.860.1839.393.120.66564.017.001.493
2385.311.360.2784.491.300.26510.244.730.96560.5810.912.227
2395.711.390.2795.251.320.26913.136.131.25160.728.541.744
2415.401.150.2354.631.130.23110.483.930.80354.3513.292.712
2465.321.000.1994.491.050.2109.973.940.78862.226.811.362
2484.761.270.2533.791.230.2467.923.550.71058.4612.702.540
2555.291.300.2654.681.600.32610.966.281.28151.0913.832.823
2564.730.950.1983.820.950.1977.662.580.53763.147.151.491
2574.761.000.2043.721.080.2207.653.450.70562.746.961.420
2594.911.190.2544.151.160.2478.774.000.85261.268.781.873
2615.430.890.1864.601.000.20910.313.720.77557.6211.732.447
2655.481.010.2074.681.250.25510.763.930.80262.478.701.775
2675.821.180.2454.891.230.25711.914.991.04156.339.261.932
2705.301.060.2264.400.980.2099.693.860.82256.8818.173.874
2714.981.180.2404.101.170.2458.934.160.86661.0511.972.444
2755.020.970.1994.351.120.2289.163.240.66159.638.161.665
2795.150.930.1984.050.840.1798.602.820.60064.836.151.311
2824.961.280.2804.141.280.2808.913.880.84763.339.762.130
2836.241.190.2486.181.630.34017.138.221.71442.6716.593.460
2865.061.240.2594.331.260.2629.464.610.96255.4512.912.691
2874.930.950.2024.201.200.2568.863.860.82258.509.802.090
3385.111.010.2124.361.260.2639.554.881.01757.6010.102.107
3395.261.120.2284.301.240.2539.624.300.87859.2814.572.973
3404.870.700.1464.020.770.1608.102.420.50564.968.381.747
3415.361.160.2374.821.310.26711.044.460.91152.4010.802.204
3424.441.620.3243.761.790.3588.196.241.24759.5014.212.843
3434.411.320.2703.711.120.2337.443.380.70658.8812.362.577
3454.931.290.2683.931.420.2978.644.831.00665.387.971.662
3464.781.120.2334.201.300.2708.784.320.90258.3010.572.204
3474.641.580.3223.481.570.3217.664.971.01462.278.351.704
3485.321.250.2724.311.190.2599.714.280.93366.705.901.287
3494.881.170.2454.341.150.2399.093.850.80359.2710.442.226
3505.130.970.1994.090.940.1918.743.180.65065.036.021.228
3514.621.000.2243.961.290.2888.033.560.79755.3913.162.944
3525.411.590.3314.711.780.37211.425.561.15958.5211.182.331
3535.461.460.2914.531.260.25310.565.601.11959.969.561.912
3544.771.090.2273.911.000.2097.95a3.080.64360.739.301.939
3555.131.030.2154.251.110.2329.203.790.79059.9710.462.182
3565.061.130.2304.341.320.2709.474.090.83462.506.261.277
3575.231.170.2394.451.280.26210.035.401.10359.4610.212.084
3585.021.670.3404.321.420.2969.875.651.17861.469.221.883
3594.791.050.2153.851.090.2227.923.230.65964.987.181.466
3605.020.770.1574.350.920.1889.072.900.59359.607.561.544
3615.181.450.2954.201.500.3079.675.851.19465.017.511.534
3624.720.960.1923.791.020.2057.663.000.60063.9910.662.131
3634.611.420.2953.871.450.3028.104.240.88362.217.371.538
3645.710.770.1575.171.190.24412.314.630.94555.4014.072.872
3654.561.110.2263.431.030.2106.86a2.670.54566.1510.112.063
3664.651.470.3004.061.480.3038.604.660.95157.828.731.782
3674.851.230.2514.121.340.2748.774.300.87759.3311.422.382
3685.540.870.1774.450.820.1679.983.130.63865.955.101.040
3704.741.130.3034.041.170.3118.303.660.97861.014.221.127
3724.800.850.1854.241.310.2878.804.000.87255.7111.002.401
3774.530.940.2003.570.970.2067.033.000.63960.887.291.555
3795.280.970.1944.361.050.2109.603.950.79061.448.641.728
3805.361.480.3094.501.040.22110.373.780.80663.729.331.946
3815.300.890.1864.811.070.22310.643.640.75957.327.761.619
3845.061.220.2444.481.520.3059.974.920.98460.1011.182.237
3885.131.350.2764.131.310.2679.133.690.75364.439.021.881
3895.501.110.2224.381.100.22010.054.580.91662.287.691.538
3904.941.150.2394.161.010.2108.703.390.70762.997.891.645
3915.470.990.2034.591.100.22510.464.130.84264.304.300.878
3934.241.450.3033.641.540.3277.464.340.92560.8710.102.106
3955.310.890.2394.510.940.2529.893.791.01460.348.062.153
4024.701.150.2353.631.110.2277.443.270.66766.097.171.464
4035.091.130.2474.191.280.2799.143.980.86862.3112.542.736
4044.671.110.2323.821.210.2537.843.640.75961.369.141.906
4055.051.160.2314.141.130.2258.913.900.77957.3614.282.856
4064.621.360.2843.861.490.3128.185.121.06761.648.991.875
4075.041.470.3074.121.250.2619.034.500.93860.1412.512.609
4085.061.090.2274.241.340.2809.223.930.81963.207.071.474
4104.961.250.2674.001.360.2918.755.001.06564.1311.952.547
4115.521.350.2704.831.620.32511.806.831.36653.2916.843.368
4125.441.090.2334.581.350.28910.685.781.23259.3511.572.467
4235.181.350.2964.541.500.32710.355.221.13958.6911.582.526
4243.941.460.3443.021.270.2985.813.700.87263.7713.403.159
4253.280.440.1392.280.430.1373.740.740.23563.257.462.359

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Pérez, S.; Renedo, C.J.; Ortiz, A.; Ortiz, F.; Santisteban, A. Biomass Losses Caused by Teratosphaeria Leaf Disease in Eucalyptus globulus Short Rotation Forestry. Forests 2017, 8, 447. https://doi.org/10.3390/f8110447

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Pérez S, Renedo CJ, Ortiz A, Ortiz F, Santisteban A. Biomass Losses Caused by Teratosphaeria Leaf Disease in Eucalyptus globulus Short Rotation Forestry. Forests. 2017; 8(11):447. https://doi.org/10.3390/f8110447

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Pérez, Severiano, Carlos J. Renedo, Alfredo Ortiz, Félix Ortiz, and Agustín Santisteban. 2017. "Biomass Losses Caused by Teratosphaeria Leaf Disease in Eucalyptus globulus Short Rotation Forestry" Forests 8, no. 11: 447. https://doi.org/10.3390/f8110447

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