172,620
Views
88
CrossRef citations to date
0
Altmetric
Articles

The effects of organic manure and chemical fertilizer on the growth and nutrient concentrations of yellow poplar (Liriodendron tulipifera Lin.) in a nursery system

, , , &
Pages 137-143 | Received 29 Jul 2015, Accepted 14 Dec 2015, Published online: 11 Apr 2016

Abstract

Soil nutrient management is necessary to maintain the constant productivity of nursery systems as well as good quality soil. This study investigated the effects of organic manure and chemical fertilizer treatments on growth performance and soil and tissue chemical properties. Two-year-old yellow poplar (Liriodendron tulipifera L.) seedlings were treated with an organic manure (1000 g/m2; mixture of poultry manure, cattle manure, swine manure, and sawdust), nitrogen–phosphorus–potassium (NPK) chemical fertilizer (urea, 30 g/m2; fused superphosphate, 70 g/m2; potassium chloride, 15 g/m2), and organic manure plus NPK chemical fertilizer. Control seedlings were left untreated. Growth of seedlings, soil properties, and nutrient concentrations were measured to compare the treatments. Organic manure significantly increased the soil pH and the concentrations of nitrogen, available phosphorus, exchangeable potassium, calcium, and magnesium. In contrast, the NPK chemical fertilizer decreased the soil pH and exchangeable calcium concentration, did not affect the soil concentrations of nitrogen and magnesium, and increased the concentrations of available phosphorus and exchangeable potassium. Fertilization treatments increased the seedling height and root collar diameter by 21% and 29%, respectively, and the mean dry weight of the stems and leaves by 72% and 123%, respectively; but a synergistic effect of the organic manure and NPK fertilizer was not observed. Compared to the effects of the fertilization treatments on the soil properties, the effects on nutrient concentrations in the leaves, stems, and roots were relatively small. These findings indicate that organic manure derived from livestock byproducts and sawdust can be utilized in seedling production systems.

Introduction

The use of chemical fertilizers and organic manure has both positive and negative effects on plant growth and the soil. Chemical fertilizers are relatively inexpensive, have high nutrient contents, and are rapidly taken up by plants. However, the use of excess fertilizer can result in a number of problems, such as nutrient loss, surface water and groundwater contamination, soil acidification or basification, reductions in useful microbial communities, and increased sensitivity to harmful insects (Chen Citation2006). Organic manure has a number of shortcomings, including low nutrient content, slow decomposition, and different nutrient compositions depending on its organic materials, compared to chemical fertilizers. However, organic manure has multiple benefits due to the balanced supply of nutrients, including micronutrients, increased soil nutrient availability due to increased soil microbial activity, the decomposition of harmful elements, soil structure improvements and root development, and increased soil water availability.

In agricultural fields, organic manure that is produced from animal byproducts has been utilized to overcome environmental contamination and plant productivity reductions that result from the constant utilization of chemical fertilizers. Recycling waste from the livestock industry prevents environmental contamination and reduces treatment costs. At the same time, it promotes soil improvements and agricultural productivity. However, the simultaneous use of chemical fertilizer and organic manure has revealed diverse results relative to the plant types and soil characteristics. Chand et al. (Citation2006) have reported that the mixed use of nitrogen–phosphorus–potassium (NPK) chemical fertilizer and livestock organic manure increases the mean growth of mint (Mentha arvensis) and mustard (Brassica juncea) by 46% and the soil concentrations of nitrogen, phosphorus, and potassium by 36%, 129%, and 65%, respectively. Kaur et al. (Citation2005) compared the use of chemical fertilizer treatment only and mixed chemical fertilizer and organic manure treatment in farmland rotating sorghum (Pennisetum glaucum) and wheat (Triticum aestivum), and found that organic manure increased the soil concentrations of organic carbon, nitrogen, phosphorus, and potassium, thus highlighting its importance in tropical farmland, which lacks organic matter. A study on tomatoes (Lycopersicon esculentum) and corn (Zea mays) in acidic soil by Murmu et al. (Citation2013) found that organic manure increases crop productivity, nitrogen utilization efficiency, and soil health compared to chemical fertilizer. Most studies in agricultural fields have reported that the mixed use of chemical fertilizer and organic manure decreases the damage that can be induced by chemical fertilizers and improves crop productivity.

Fewer studies have been performed in forestry fields compared to agricultural fields. In a study on a short-rotation willow (Salix dasyclados) plantation that was carried out to maximize biomass production in the middle east region of North America, using slow-acting chemical fertilizer and organic livestock manure, the organic manure treatment markedly increased the growth of the willow, the pH at a soil depth of 0–10 cm by 2, and soil concentrations of potassium, phosphorus, and magnesium (Adegbidi et al. Citation2003). However, Larcheveque et al. (Citation2011) found that chemical fertilizers promote higher growth and root development compared to livestock organic manure in a poplar plantation in clay soil.

To maintain consistently high biomass productivity, soil nutrient management is essential, and fertilization is the only way to supply soil nutrients within a short period of time. Adegbidi et al. (Citation2003) reported that fertilization costs accounted for 20%–30% of the total production costs in biomass production. However, the effects of the mixed use of chemical fertilizer and organic manure on the growth of trees and soil fertility vary substantially according to the fertilizer amounts and the organic manure characteristics. The amount of organic manure required is mainly determined by the nitrogen content. However, special attention needs to be paid because the ratios of nutrients other than nitrogen can differ from the trees’ requirements.

Yellow poplar (Liriodendron tulipifera L.) is highly adaptable to the climate in Korea. It grows rapidly and has been widely utilized in timber production and landscaping. In addition, due to its high carbon absorption capacity, yellow poplar is the major tree species used in reforestation for the formation of bio-circulation forests in order to replace fossil fuels and secure Certified Emission Reductions (Ryu et al. Citation2003, Citation2008).

The objective of this study was to investigate the effects of chemical fertilizer and organic manure treatments on the growth of yellow poplar seedlings and soil characteristics. We hypothesized that organic manure would be comparable to that of chemical fertilizer on seedling growth because of its indirect effect on soil property improvement. By evaluating the possibility of the utilization in forestland of organic manure produced as animal byproducts, which can be continually utilized in soil for a long time, the findings of this study help to suggest ways to increase seedling productivity.

Materials and methods

Study sites and species

This study was performed in the Forest Practice Research Center of Korea Forest Research Institute, which is located in Pocheon, Gyeonggi Province (37°45ʹ N, 127°09ʹ W). The mean annual temperature is 11.3 °C, and the annual precipitation is 1365 mm.

For the experimental treatments (), the nursery was plowed deeper than 30 cm and installed in a 1 m × 20 m nursery bed in an east–west direction. Nursery beds were separated by 50 cm, and a buffer zone greater than 40 cm separated the treatment plots. In order to measure the physical and chemical properties of the soil before the experiments, three points were randomly selected, and 500 g samples of soil were collected at soil depths of 0–10 cm and 10–30 cm. For the study species, a yellow poplar named as Kentucky 1-0 seedling that was produced by the Forest Genetic Resources Department of Korea Forest Research Institute was used. In order to prevent the roots from drying, the harvested seedlings were covered by soil and straw mats and were provided with sufficient water until the following planting day. The seedlings were planted in beds with a width of 25 cm and vertical length of 14 cm (35 seedlings/m2), and the stems were cut at a height of 5 cm from the ground. To aid initial rooting, water was provided every day for 2 weeks after planting.

Experimental treatments

Organic manure consisting of 20% poultry manure, 10% cattle manure, 20% swine manure, and 50% sawdust (Production registration 10-[19]-B-1-5) was used in this study. Two 20 kg bags were randomly selected to measure the moisture (47.1%), nutrient, and heavy metal content (). For the chemical fertilizer, NPK fertilizer consisting of a mixture of the major components of nitrogen, phosphorus, and potassium (urea, 60 g/m2; fused superphosphate, 140 g/m2; potassium chloride, 30 g/m2) was used. The organic manure and chemical fertilizer were applied 6 weeks after planting. Nursery beds were assigned to the organic manure treatment, the NPK fertilizer treatment, the organic manure and NPK fertilizer treatment, or the untreated control group according to a completely randomized block design with 2 × 2 factorial, with 8 replicates in total (). The fertilizer was evenly distributed by hand between the seedlings and mixed well with the soil. A boundary was installed on the edges of the treatment sections using wooden boards that were placed to a depth of 5 cm and a height of 5 cm from the ground in order to prevent fertilizer loss due to rainfall.

Table 1. Properties of fertilization treatments.

Table 2. Chemical properties of applied manure compost.

Table 3. Soil properties before fertilization treatments.

Growth measurements

Growth measurements on the aboveground and belowground part were performed 20 weeks after the fertilization treatments. Except for the seedlings that were planted on the edges of the treatment sections, four seedlings were randomly selected from the inside of the treatment plots in order to minimize edge effects. In order to minimize root damage during harvesting, seedlings on the edges were harvested first, and the rest were then harvested in a way to avoid fine root cutting by removing the soil inside.

The root diameters and heights of the harvested seedlings were measured, and the roots were then washed with running water more than three times to remove the soil on the root surface. The aboveground part was collected by dividing stems, branches and leaves, and the belowground part was collected without dividing it into taproots and fine roots. The collected samples were dried at 65 °C for 1 week, and their dry weights were then measured.

Soil and plant tissue analysis

Prior to the seedling harvest, soil samples were collected to analyze the chemical properties of the soils exposed to the different treatments (). After the random selection of two points in all of the treatment sections, excluding the edges, the leaves that had fallen on the soil surface were removed, and 500 g of soil was collected at a depth of 0–10 cm. After the sampling, two samples from each treatment were mixed, and a soil analysis was conducted. The analyses were replicated four times for each treatment. The samples for the plant nutrient analysis were collected from the seedlings that were used in the dry weight measurements. The plant nutrient analyses were replicated four times for each treatment.

The soil, organic manure, and plant samples were analyzed as follows. The collected soil was air-dried at room temperature, and the soil texture, pH, organic matter content, total nitrogen, available phosphorus, and exchangeable potassium, calcium, magnesium, sodium, cation exchange capacity (CEC), and electric conductivity (EC) were measured. The soil texture was measured at a constant temperature of 30 °C with the hydrometer method, and the organic matter content was analyzed with the Tyurin method which is a wet combustion method. To measure soil pH, 10 g of soil was mixed with distilled water at a ratio of 1:5, and the pH was measured with a pH meter. The total nitrogen content was measured in 1 g of soil with the Micro-Kjeldahl method. The available phosphorus (P2O5) in the soil was measured with the Lancaster method. Exchangeable potassium, calcium, magnesium, and sodium were eluted with 1 N NH4OAc and then measured with an Atomic Absorption Spectrometer (AA280FS). CEC was measured in 10 g of soil in 1 N NH4OAc and 1 N CH3COOH solvents with the Brown method.

Statistic analyses

Tukey's multiple comparison tests were used to analyze the soil properties, plant nutrient concentrations, and growth performances after treatment. The tests were performed at a 5% significance level (SAS 9.3). Statistical analyses of the seedling height, root diameter, and dry weight were implemented at a 5% significance level with a covariate analysis that considered the initial growth values.

Results and discussion

Soil chemical properties

The NPK fertilizer treatment significantly decreased soil pH, whereas organic manure treatments significantly increased soil pH (). Soil nitrogen content increased by 17% after the organic manure treatment, while soil nitrogen content after NPK fertilizer treatment was similar to that of the control group. The available phosphorus in the soil increased more than 50% in all treatments. Similar to available phosphorus, exchangeable potassium concentrations were significantly increased in all treatments, more than doubling after organic manure treatment. Exchangeable calcium was reduced after NPK fertilizer treatment, and no changes were exhibited in the magnesium concentrations. However, the organic manure treatment significantly increased both the calcium and magnesium concentrations in the soil. Electrical conductivity was increased after the organic manure and NPK fertilizer treatments, and the highest electrical conductivity was observed in the soil treated with the combined organic manure and NPK fertilizer.

Table 4. Soil properties after fertilization treatments.

The results of this study were in agreement with the results of several studies that have shown organic manure treatment increased soil pH, but chemical fertilizer treatments, such as NPK fertilizer, decreased soil pH (Warren Fonteno Citation1993; Whalen et al. Citation2000; Liu et al. Citation2010). The decrease of soil pH by NPK fertilizer may be explained by leaching of basic cations, such as potassium, calcium, and magnesium from the soil. However, Chang et al. (Citation1990) reported that soil pH decreased by 0.3–0.7 after 11 years of organic manure treatment (with livestock byproducts) at base rich soil, and that the decrease was greater when the amount of manure treatment was increased. Another study reported that long-term treatments with anaerobic swine lagoon liquid reduced the soil pH by 0.97 (from 6.9 to 5.93 in Brooksville soil), 0.11 (from 7.5 to 7.39 in Okolona soil), and 0.88 (from 5.4 to 4. 52 in Vaiden soil) (Adeli et al. Citation2008). Generally, organic manure with livestock byproducts increases soil pH, but the effects differ depending on the organic matter content, treatment amounts, and soil properties. Although this study did not analyze soil calcium carbonate after the fertilization treatments, calcium carbonate that is increased by organic manure treatments is believed to increase buffering, thereby increasing the soil pH (Eghball Citation1999).

Similar to other studies, NPK fertilizer treatment acidified the soil because the urea that was used in this study was used by the plants as NH4+ first and then the H+ was released into soil, which thereby decreased the soil pH (Magdof et al. Citation1997). This process reduces most of the activities of bacteria and actinomycetes in the soil (Kaur et al. Citation2005) and seems to be the cause of soil cations leaching over the long term (Likens et al. Citation1996; Bailey et al. Citation2004). The long-term utilization of NPK fertilizer eventually results in deficiencies in other essential nutrients, which may deteriorate the physical, chemical, and biological properties of the soil.

A total of 30% organic matter content in organic manure is believed to increase the content of nitrogen, phosphorus, potassium, and main cations in the soil (). The organic matter of manure allows plants to use the nutrients for a long time, due to its slow decomposition, and reduces the loss of what is not utilized by the plants (Bhandari et al. Citation2002). In the present study, the phosphorus content of the soil was increased by the organic manure and the chemical fertilizer, indicating that the plant was not able to utilize a large quantity of the phosphorus that was provided by fertilization and that it accumulated on the soil surface, as reported by Singh et al. (Citation2007). Major cations, including potassium, and nitrogen and phosphorus were increased by organic manure treatment due to their high content in organic manure.

Growth and nutrient responses

All fertilization treatments increased the seedlings height () and root collar diameter () by 29% and 21%, respectively, but no significant differences were found among the fertilization treatments. Fertilization treatments significantly increased the mean dry weight of the stems and leaves by 72% and 123%, respectively, compared to the control, and the root dry weight was increased by 18%, which was not significant (). This indicated that the fertilization treatments affected carbohydrate distribution in the plants. The proportion of the belowground to the aboveground part in the control was 85%, but this was decreased to 47%–55% by the fertilization treatments. In addition, the dry weight proportion of the leaves of the aboveground part was significantly increased by the fertilization treatment.

Figure 1. Height growth of Liriodenron tulipifera after treatments of manure compost and NPK fertilizer. Means with the same letter are not significantly different among treatments at α = 0.05. Vertical bars represent one standard error of the mean (n = 4).

Figure 1. Height growth of Liriodenron tulipifera after treatments of manure compost and NPK fertilizer. Means with the same letter are not significantly different among treatments at α = 0.05. Vertical bars represent one standard error of the mean (n = 4).

Figure 2. Root collar diameter growth of Liriodenron tulipifera after treatments of manure compost and NPK fertilizer. Means with the same letter are not significantly different among treatments at α = 0.05. Vertical bars represent one standard error of the mean (n = 4).

Figure 2. Root collar diameter growth of Liriodenron tulipifera after treatments of manure compost and NPK fertilizer. Means with the same letter are not significantly different among treatments at α = 0.05. Vertical bars represent one standard error of the mean (n = 4).

Figure 3. Biomass growth of Liriodenron tulipifera after treatments of manure compost and NPK fertilizer. Means with the same letter are not significantly different among treatments at α = 0.05. Vertical bars represent one standard error of the mean (n = 4).

Figure 3. Biomass growth of Liriodenron tulipifera after treatments of manure compost and NPK fertilizer. Means with the same letter are not significantly different among treatments at α = 0.05. Vertical bars represent one standard error of the mean (n = 4).

Fertilization treatments significantly increased the growth of the yellow poplar, but a synergistic effect of the organic manure and NPK fertilizer was not observed (). The amounts of nitrogen, phosphorus, and potassium that were supplied by the NPK fertilizer treatment were 27.6, 12.2, and 15.0 g/m2, respectively () while those supplied by organic manure were less by 34%, 41%, and 20%, respectively, than those of NPK fertilizer. However, similar growth patterns were seen after organic manure treatment because of the increased nutrient availability that occurred by the supply of other essential nutrients and the by improvements in the quality of the soil due to the pH increase, even though the amounts of nitrogen, phosphorus, and potassium were relatively small. Murmu et al. (Citation2013) and Tomati et al. (Citation1988) found that vermicompost, which is an organic manure, provides not only major elements and trace elements that are necessary for the plant but also plant growth regulators and humic acid, which facilitate plant growth. The results of this study showed that only the utilization of organic manure, without NPK fertilizer, could maintain biomass productivity at a level similar to NPK fertilizer and enhance the quality of soil.

Whereas the fertilization treatment significantly influenced the soil nutrients (), it hardly affected the leaves and stems of the plant or the nutrient concentrations of the roots (). The nitrogen concentration was not changed in the stems and leaves by the treatment, but a significant increase was observed in the roots by the fertilization treatment. Phosphorus tended to decrease in the leaves and roots after fertilization treatment. The magnesium concentration in the leaves was decreased by the fertilization treatment, and the other remaining nutrients and organs did not exhibit a significant trend in response to fertilization treatment.

Table 5. Foliage nutrient concentrations after treatments.

Findings of no substantial changes in nutrient concentrations after fertilization treatment have been reported in other studies (Park et al. Citation2012; Park et al. Citation2013). These findings suggest that fertilization treatment increases the available nutrients in the soil, that biomass production is increased by the nutrients which are absorbed by the plant, thereby resulting in no changes in the plant nutrient concentrations in the tissues, which corresponds to “adequate (arrow B)” in the nutrient vector analysis by Timmer (Citation1996). The actual nitrogen content by fertilization treatment is very high. The contents of organic manure, NPK fertilizer, and NPK fertilizer plus organic manure treatment were 191%, 224%, and 198%, respectively, and phosphorus and potassium showed similar content patterns.

Conclusions

Soil nutrient management is essential for sustainable biomass production and for maintaining soil quality. Organic manure increased soil pH, the concentrations of nitrogen, phosphorus, and major cations. The growth of yellow poplars by organic manure treatment is comparable to that of NPK fertilizer treatment. Prior to applying livestock byproduct-derived organic manure, the different nutrient compositions of the organic manures by the types of livestock byproducts, the soil properties of the application lands, the nutrient requirements of the target tree species, and environmental and sanitary conditions in surrounding areas should be taken into consideration. This study confirmed that organic manure originating from livestock byproducts and sawdust not only promoted the growth of yellow poplar but also improved soil conditions. Therefore, organic manure should be considered as an alternative to chemical fertilizers in nursery seedling production systems.

Acknowledgements

We thank Dr. Jae Kyung Byun for helping us design this experiment. We also thank Dr. Soo Won Lee, Mr. Wonguk Kim, and Ms. Youngsun Min for their help with the field work and water irrigation at the nursery.

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This study was partly carried out with the support of the Research Fund of Chungnam National University.

References

  • Adegbidi HG, Briggs RD, White EH, Abrahamson LP, Volk TA. 2003. Effect of organic amendments and slow-release nitrogen fertilizer on willow stem biomass production and soil chemical characteristics. Biomass Bioenergy. 25(4):389–398.
  • Adeli A, Bolster CH, Rowe DE, McLaughlin MR, Brink GE. 2008. Effect of long-term swine effluent application selected soil properties. Soil Sci. 173(3):223–235.
  • Bailey SW, Horsley SB, Long RP, Hallett RA. 2004. Influence of edaphic factors on sugar maple nutrition and health on the Allegheny plateau. Soil Sci Soc Am J. 68(1):243–252.
  • Bhandari AL, Ladha JK, Pathak H, Padre AT, Dawe D, Gupta RK. 2002. Yield and soil and nutrient changes in a long-term rice-cowpea cropping system in semi-arid tropics. Plant Soil. 318:27–35.
  • Chand S, Anwar M, Patra DD. 2006. Influence of long-term application of organic and inorganic fertilizer to build up soil fertility and nutrient uptake in mint‐mustard cropping sequence. Commun Soil Sci Plant Anal. 37(1-2):63–76.
  • Chang C, Sommerfeldt TG, Entz T. 1990. Rates of soil chemical changes with eleven annual applications of cattle feedlot manure. Canadian J Soil Sci. 70(4):673–681.
  • Chen JH. 2006. The combined use of chemical and organic fertilizers and/or biofertilizer for crop growth and soil fertility. Proceedings of International Workshop on Sustained Management of the Soil-Rhizosphere System for Efficient Crop Production and Fertilizer Use. Available from http://www.agnet.org/htmlarea_file/library/20110808103954/tb174.pdf
  • Eghball B. 1999. Liming effects of beef cattle feedlot manure or compost. Commun Soil Sci Plant Anal. 30(19-20):2563–2570.
  • Kaur K, Kapoor KK, Gupta AP. 2005. Impact of organic manure with and without mineral fertilizers on soil chemical biological properties under tropical conditions. J Plant Nutr Soil Sci. 168(1):117–122.
  • Korea Forest Service. 2012. Guidelines on seedling practice. (In Korean). Daejeon: Korea Forest Service.
  • Larcheveque M, Desrochers A, Larocque GR. 2011. Comparison of manure compost and mineral fertilizer for hybrid poplar plantation establishment on boreal heavy clay soils. Ann For Sci. 68(4):849–860.
  • Likens GE, Driscoll CT, Buso DC. 1996. Long-term effects of acid rain: response and recovery of a forest ecosystem. Science. 272(5259):244–246.
  • Liu E, Yan C, Mei X, He W, Bing SH, Ding L, Liu Q, Liu S, Fan T. 2010. Long-term effect of chemical fertilizer, straw, and manure on soil chemical and biological properties in northwest China. Geoderma. 158(3):173–180.
  • Magdof F, Lanyon L, Liebhardt B. 1997. Nutrient cycling, transformations and flows: implications for a more sustainable agriculture. Adv Agron. 60:1–73.
  • Murmu K, Swain DK, Ghosh BC. 2013. Comparative assessment of conventional and organic nutrient management on crop growth and yield and soil fertility in tomato-sweet corn production system. Aust J Crop Sci. 7(11):1617–1626.
  • Park BB, Byun JK, Sung JH, Cho MS. 2013. Study of optimal fertilization with vector analysis in hardwood and softwood seedlings. J Agric Life Sci. 47(5):95–107.
  • Park BB, Cho MS, Lee SW, Yanai RD, Lee DK. 2012. Minimizing nutrient leaching and improving nutrient use efficiency of Liriodentron tulipifera and Larix leptolepis in a container nursery system. New Forests. 43(1):57–68.
  • Ryu KO, Jang SS, Choi WY, Kim HE. 2003. Growth performance and adaptation of Liriodendron tulipifera in Korea. J Korean For Soc. 92 (6):515–525. (In Korean with English abstract)
  • Ryu KO, Kim UJ, Kim IS, Choi HS, Lee DH, Kim YW. 2008. Liriodendron tulipifera L. – growth characteristics and utilization technique. Korea Forest Research Institute; p. 320. (In Korean)
  • Singh M, Reddy SR, Singh VP, Rupa TR. 2007. Phosphorus availability to rice (Oriza sativa L.)-wheat (Triticum estivum L.) in a Vertisol after eight years of inorganic and organic fertilizer additions. Bioresource Tech. 98(7):1474–1481.
  • Timmer VR. 1996. Exponential nutrient loading: a new fertilization technique to improve seedling performance on competitive sites. New Forests. 13(1-3):275–295.
  • Tomati U, Grappelli A, Galli E. 1988. The hormone-like effect of earthworm casts on plant growth. Biol Fert Soils. 5(4):288–294.
  • Warren SL, Fonteno WC. 1993. Changes in physical and chemical properties of a loamy sand soil when amended with composted poultry litter. J Environ Hortic. 11:186–190.
  • Whalen JK, Chang C, Clayton GW, Carefoot JP. 2000. Cattle manure amendments can increase the pH of acid soils. Soil Sci Soc Am J. 64(3):962–966.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.