Interaction of precipitation with tree canopy increases nutrient input

Given that atmospheric deposition is the first source of nutrient input into forest ecosystems, and that the precipitation partition serves as a nutritional source mainly when there is an interaction with the forest canopy, the objective of the present study was to quantify the nutrients input into rainfall, throughfall and stemflow in Eucalyptus urophylla stands with partial exclusion (E) and without exclusion (WE) of throughfall. The experiment was conducted in the northeast of the state of Paraná-Brazil, in the municipality of Telêmaco Borba. The partial precipitation exclusion system (E) is formed by a system of gutters that conduct 30% of throughfall out of the experiment. The nutrient input in rainfall was 55.7 kg ha yr, while the sum of throughfall and stemflow was 64.1 kg ha yr in treatment (WE) and 39.8 kg ha yr in treatment (E). Interaction with the canopy of the trees enriched the rainfall with nutrients, mainly the elements potassium and chlorine, due to leaching of the vegetal tissues. The reduction of the water treatment system in partial exclusion of precipitation (E) reduced representative nutrient input. Although stemflow represents on average only 2.6% of the water volume, it is responsible for 6.7% of the amount of nutrients in relation to precipitation. Therefore, stemflow cannot be neglected in the balance of nutrient cycling. With a rotation of 7 years, the application of significant amounts of fertilizers can be avoided, considering the inputs of 449 and 277 kg hayear.


INTRODUCTION
The forestry sector has occupied a prominent position in the Brazilian economy. Planted forests occupy 9.0 million hectares of the country and the genus Eucalyptus represents 77% of this area. Even with the large area occupied, the industrial forest plantations cover about 0.92% of the Brazilian territory. Paper and cellulose commodities occupy the second place in the list of products most exported by Brazil (IBÁ, 2020).
Extensive areas occupied by forest plantations are able to modify the hydrological balance (Ferraz et al. 2019). The partition of the rainfall in the area covered by vegetation is very dynamic. During precipitation, a portion of the water is intercepted by the canopy and immediately evaporated into the atmosphere (Llorens and Domingo, 2007). Part of the precipitation crosses the canopy and drips into the stand; this is called "throughfall" (Navar, 2011). A portion of the throughfall flows from the leaves to the branches and trunk, reaching the base of the tree; this portion is called "stemflow" (Zhang et al., 2016;Johnson and Lehmann, 2006). The knowledge of the partition of precipitation is important in studies of modeling the water balance of a watershed; however, many studies have considered a generic value for the index of canopy interception (Chaffe et al., 2010).
Many studies show the importance of the partition of precipitation in the biogeochemical cycle of nutrients (Staelens et al., 2006;Fan et al., 2015). Some studies also point out that the productivity and stability of a forest ecosystem is determined by the cycling of nutrients (Likens 2013). According to Viera and Schumacher (2010), part of the input of nutrients into an ecosystem occurs through precipitation that carries dust particles from the atmosphere to the ground. In addition, when interacting with the canopy of the trees, precipitation leaches the different tissues of the plant, increasing the nutritional contribution (Schrumpf et al., 2006;Bhat et al., 2011;Levia et al., 2011). Thus, precipitation is responsible for providing information regarding environmental quality (Zhou et al., 2019). In addition, soils from areas of low natural fertility, the entry of nutrients by precipitation may be the only nutritional source (Dawoe et al., 2018;Lu et al., 2017).
The chemical composition of throughfall and stemflow is influenced by the interaction of water with the forest canopy, distance from the sea and anthropogenic activities (Andre et al., 2008;Navar et al., 2009;Tiwari et al., 2016). In general, these pathways provide an important

Characterization of the experimental area
The experimental area is located in the northeast region of the state of Paraná, in the municipality of Telêmaco Borba, under the geographic coordinates 24°13'41.0" S and 50°31'40.0" W. The climate classification is Cfb (temperate climate), with an average annual temperature of 18.8ºC and an average annual precipitation of 1646 mm, according to the Köppen classification (Alvares et al., 2014). According to Flores et al. (2016) the species E. urophylla is classified as having low climatic aptitude for the study region. Figure 1 shows meteorological data for the period from July 2017 to June 2018, obtained from the meteorological station located at the company Klabin SA in Telêmaco Borba -PR -Brazil at 880 m altitude, 24°12'40.6" S and 50°33'29.2" W. The distance between the experimental area and the weather station is approximately 3.4 km in a straight line. In March 2017, dendrometric characterization was performed, measuring the height and diameter at breast height (DBH) of all trees. The mean DBH and the total height in the Exclusion (E) treatment were 16.8 cm and 28.6 m, respectively. For the Without Exclusion (WE) treatment, the mean DBH was 17.3 cm and the total height 28.3 m. The volume per hectare in the E and WE treatment was 346 and 365 m³ ha -1 , respectively. The leaf area index was 2.95 and 2.82 for treating exclusion (E) and without exclusion (WE), respectively.

Experimental design
The study belongs to the TECHS project (Tolerance of Eucalyptus Clones to Hydric, Thermal and Biotic Stresses). The experiment was carried out in a completely randomized design, with 720 m² plots of eight lines with ten plants each in spacing of 3 m x 3 m (1,111 trees ha-1). For the hybrid E. urophylla x E. sp. two treatments of the water regime were defined: one receiving 100% of the throughfall (WE) and the other receiving only 70% of the throughfall (E). For the treatment (E) that received 70% of the precipitation, a system of partial exclusion of the throughfall was used with plastic gutters that prevented the precipitation reaching the ground. A schematic representation of the precipitation exclusion treatment (E) can be seen in Figure 2. This technique is based on the coverage between the planting lines covering 216 m² of the area of each treatment, being the equivalent to 30% of the plot area (Binkley et al., 2017). The monitoring of the partition of precipitation under the two rainfall regimes occurred from July 2017 to June 2018. Sampling was started when the stand was 66 months old. For the (E) treatment, a partial exclusion system of throughfall was used, installed when the stand was one year old.

Measurement of rainfall, throughfall and stemflow
To quantify the rainfall (R), three collectors with a 20 cm catchment diameter were installed in an area adjacent to the eucalyptus stand at a height of 1.5 m above ground level. Straps with steel wires were placed in order to prevent birds from using the collectors as perches.
For the evaluation of throughfall (Tf), nine collectors per treatment were installed, with a collection diameter of 20 cm and height of 1 m from ground level, systematically distributed along the line, between the lines and diagonally between four trees. Collections were started at 66 months of age. The stemflow quantification (Sf) occurred with the installation of nine sets formed by a plastic hose with a diameter of one inch and a reservoir for water storage. The hose was cut longitudinally and then it was installed in a spiral shape on the tree trunk. This configuration allowed the water to drain through the trunk and be stored in the reservoir.
Bi-weekly, the values of rainfall (R), throughfall (Tf) and stemflow (Sf) were measured. To obtain the values of precipitation and throughfall in millimeters, the following Equation 1 was used: For the canopy interception calculation, the Equation 3 was used: Where: The rainfall and throughfall collectors were composed of plastic bottles with a capacity of 2 liters, and the collections were carried out every 15 days. The throughfall collectors were arranged on the line, between the lines and diagonally between four trees. The stemflow samples were also collected for chemical analysis every 15 days.

Statistics and Data Analysis
The rainfall, throughfall and stemflow samples were sent to the Forest Ecology Laboratory where the pH was determined. For this variable, the electrode (Methohm 827 pH LAB) was used, and filtered with a 0.45 µm pore filter. According to the methodology proposed by the American Public Health Association (APHA et al.,1998), NO2 -, NO3 -, PO4 3-, SO4 -, Cl -, K + , Ca 2+ and Mg 2+ ions were analyzed, with a pre-treatment with simple filtration followed by ion chromatography. The amount of nutrient input is given by multiplying the concentrations of ions (mg L -1 ) by the volume (liters).
The Tukey average test was performed at 5% probability of error for ion concentrations between precipitation, throughfall and stemflow. In order to verify the dilution effect, Pearson's correlations were applied between the volumes of rainfall partitions and the concentrations of ions. All statistical analyses were performed using SPSS 18.0 (SPSS Inc., Chicago, IL, USA).

Rainfall partitioning
During the monitored period, the quantified precipitation was 1627 mm. The month of December 2017 had the highest volume of R 371 mm, while the months of July 2017 and April 2018 registered the lowest volumes (0.00 and 21 mm) (Figure 3). Regarding throughfall, the WE treatment showed 1379 mm, equivalent to 84.8% of the precipitation. In contrast, the E treatment showed a lower value (1311 mm), corresponding to 80.6% of the precipitation. The volume collected for the Sf WE treatment was 48.40 mm, representing 2.9% of the rainfall. For the Sf E treatment, 37 mm was accumulated, corresponding to 2.3% of the rainfall. In the canopy interception, the lowest observed value was   (Poleto et al., 2021).

Chemical composition of rainfall, throughfall and stemflow
In the evaluated period (Figure 3), the average pH value of rainfall was 6.17. The throughfall for the E and WE treatment of the throughfall was 5.94 and 5.96, respectively. Stemflow provided an average of 4.92 and 4.55 for the E and WE treatment of throughfall ( Figure 4).  Momolli (2019b) found mean pH values of 4.57 for rainfall, 4.64 for throughfall and 5.54 for stemflow evaluation in a 7 to 8-year-old Eucalyptus dunnii stand in Alegrete, RS. Assessing the same species, from 4 to 5 years old, Dick et al. (2018) also found an increase in pH as precipitation interacts with the canopy. The pH was 4.3 in rainfall, 5.0 in the throughfall and 5.3 in the stemflow, respectively.
The ion concentration is variable as it interacts with the forest canopy. The SO4 2and Ca 2+ ions showed higher levels of rainfall, differing statistically from other rainfall partitions. Inverse behavior was observed with respect to Cl -, Na + , N-NH4 + , K + , Mg 2+ ions that registered the greatest increases, especially in Stemflow and Throughfall. The ions N-NO2and P-PO4 3showed no statistically significant difference. The mean test of the ions analyzed for each partition of the precipitation in the two water regimes can be verified in Table 1.
It is observed that the concentration of nutrients is influenced by the water regime, that is, during the months of higher rainfall, the ion concentrations are reduced while during the months of lower precipitation, the concentrations increase considerably. In the present study, the highest concentrations were recorded in the months of September, April and May, coinciding with the lowest rainfall. Other studies report the same behavior as in the case of Su et al. (2019) who monitored the chemical variation of rainwater in the different partitions in a mixed evergreen and deciduous broadleaved forest in Central China. is verified with the Pearson correlation test presented in Table 2. Mostly, a negative correlation was observed for more than 90% of the ions in the different precipitation partitions. In addition, there were strong significant correlations to a <1% error probability for K + , Ca 2+ and Mg 2+ ions and for many throughfall ions.  Figure 5 shows in detail the variation in ion concentration over the monitored period for the different partitions of rainfall. As can be seen, for most ions there are two months of prominence: September and May.

Nutrient input
The rainfall had a total nutrient input of 55.69 kg ha -1 yr -1 . For throughfall, the contribution was 60.20 kg ha -1 and 36.27 kg ha -1 for TfWE and TfE, respectively. The significant reduction in the amount of nutrients in treatment E refers to the fact that these nutrients are being carried out of the stand due to the system of excluding water from rainfall. For stemflow, the contribution was greater, with 3.96 kg ha -1 in the SfWE and 3.36 in the SfE (Figure 6). The flow of nutrients in rainfall had the following distribution order: Ca> K> Na> Cl> Mg> S> N> P. In Tf WE, the order was as follows: K> Cl> Ca> Na> Mg> N> S> P. In the Sf WE, K> Cl> Ca> Na> Mg> N> S> P. The Tf E presented the following order: K> Cl> Na> Ca> Mg> N> S> P. For SfE K> Cl> Na> Ca > Mg> N> S> P. Considering the sum of throughfall plus stemflow in the WE treatment the amount of nutrients (kg ha -1 ) was 16.6 for Cl, 0.1 for P, 1.7 for S, 8.1 for Na, 23.1 for K, 2.9 for Mg, 9.2 for Ca and 2.5 for N. As for treatment E, there was a contribution (kg ha -1 yr -1 ) of 9.3 for Cl, 0.02 for P, 1.1 for S, 5.0 for Na, 15.6 for K, 2.1 for Mg, 4.9 for Ca, 1.8 for N.
Regarding nutrient input via rainfall, it was observed that there was a significant increase in nutrients in the aqueous solution, whose input sequence was K> S> Ca> N> Mg. These inputs could reduce the addition of 22% and 11% of the amounts of K and N, respectively, applied to pre-planting fertilization (Dick et al., 2018). The annual contribution of nutrients in the present study is similar to that found by Momolli et al., (2020). For these authors, the annual contribution was 36.3 kg ha -1 . This small variation is justified according to the conditions: close to the ocean, emission of atmospheric pollutants by anthropic activity and even soil and environmental characteristics (Corti et al., 2019;Yuan et al., 2017). Possibly, the greatest  Nutrients total contribution of certain nutrients is related to the existence of two pulp mills, the first approximately 12 km away in a straight line located in the municipality of Telêmaco Borba, PR and the second approximately 21 km away in the municipality of Ortigueira, PR. Balieiro et al. (2007) in an Eucalyptus stand found a contribution (kg ha -1 ) via rainfall of 12.07 N-NH4 + ; 2.65 P; 86.00 K + ; 12.25 Ca 2+ ; 9.24 Mg 2+ ; 29.81 Na + . The increase in the amount of nutrients after interaction with the canopy is more significant for K + , which can be attributed to the high levels due to leaching of the canopy of the trees. However, some ions do not exhibit the same behavior as SO4 2-. The input via rainfall was 1.7 kg ha -1 and 1.6 kg ha -1 via TfWE. According to Gay and Murphy (1985), approximately between 30 -70% of the dry deposition of SO4 2can be retained in the canopy. Corrêa et al. (2019) evaluating an E. dunni stand 16.5 months old, found that due to the concentration of ions there was a greater contribution of elements after the interaction of precipitation with the forest canopy.

CONCLUSION
There was an enrichment of nutrients as the water interacted with the forest canopy. Considering the average levels of ions, the degree of enrichment had the following decreasing order: stemflow > throughfall > rainfall. The concentration of ions is seasonal and is especially determined by the volume of water in each partition causing the dilution effect.
The total quantity of nutrients contributed had the following order: throughfall > rainfall > stemflow. The reduction of the water treatment system in partial exclusion of precipitation (E) reduced representative nutrient input. It is important to highlight that although stemflow represents on average only 2.6% of the water volume, it is responsible for 6.7% of the amount of nutrients in relation to precipitation. Therefore, stemflow cannot be neglected in the balance of nutrient cycling.
Considering the interaction of rainwater with canopy, in a 7-year rotation there is a potential reduction of chemical fertilizers. These results point the way to greater economic and environmental sustainability.

ACKNOWLEDGEMENTS
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior -Brasil (CAPES) -Finance Code 001.

DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.