There are increasing expectations from the society for the development of an ecologically-friendly management of mineral nutrition in agro-ecosystems. Several practices and approaches could be put in place to optimize the use of external as well as internal nitrogen (N) sources, including adapting rates of fertilizers to match tree needs, adopting highly efficient technology of nutrient supply (e.g., fertigation, organic fertilization) and splitting nutrient rates are among the means to improve external N use.
It is expected that in the 21st century, the adoption of genotypes efficient in the use of nutrients, able to either incorporate more N and/or to improve its assimilation in organic forms, will play a major role for increasing crop yield and secure food for an increasing world population [1
], preserving non-renewable resources, like fertilizers, and maintaining the quality of soil. At least 60% of the world’s arable land suffers from mineral deficiencies or elemental toxicity problems [2
]. Nutrient efficient crops are those that produce high yields per unit of applied or absorbed nutrient [3
]. According to Srivastava [3
], the perennial woody nature of fruit trees, their physiological stages of growth and the differential root distribution pattern make these plants more efficient on the use of nutrients than annual crops. Although fruit trees represent about 1% of the global agricultural land, they are of a great economic importance in many regions as well as in world trade [8
]. Fruit trees, being perennial and allocating most of the net primary productivity to fruits, which contain relatively low N (Table 1
), can be managed with relatively low N supply if the orchard is properly managed.
The present paper aims (i) at reviewing the existing literature on N nutrition of young and mature deciduous and evergreen fruit trees with special emphasis to temperate and Mediterranean climates; and (ii) providing recommendations for an environmentally sustainable orchard management.
2. Tree N Uptake and Internal Cycling
Nitrogen is often regarded as the most important mineral nutrient, limiting crop production in many agricultural crops worldwide. It has a major effect on crop yield and quality. It is a component of enzymes, vitamins, the chlorophyll molecule, and is involved in nucleic and amino acid synthesis and protein production. It is important for cell division and growth of young tissues (e.g., buds, flowers, leaves, twigs). Nitrogen also affects the absorption and distribution of practically all other nutrients in the plant, and is particularly important to the tree during flowering and fruit set [9
Increasing soil and plant N availabilities enhance tree growth and vigour, two characteristics that, if managed with care are of the outmost importance for the economic success of newly planted fruit trees are therefore able to maximize their yield potential [11
]. Too much vigour can be a result of excessive soil N availability and may compromise the onset of bearing, or even the yield, in the first years. Sometimes, even when the nutrient availability is lower than the lowest threshold, trees do not respond to fertilization because of adequate nutrient reserves built up in perennial organs in previous years [9
]. Under limited available N, tree growth may appear normal but under sized. Nitrogen deficient trees carry a low fruit load and are highly erratic in their fruit bearing habit [12
]. Moreover, they flush irregularly and produce short twigs and a reduced number of pale-green leaves.
Optimal concentration of N in fruits allows a proper development of skin colour, fruit size, and flavour. In fleshy fruits, fruit N concentration is higher during the first stage of fruit development (cytokinesis) and decreases thereafter, during the fruit growth until maturity due to both a lower uptake rate and to a dilution effect. Fruit N concentration in deciduous trees depends on many factors, including grafting combination (cultivar and rootstock), environmental conditions and orchard management, and generally vary from 2.5 to 9.8 g N kg−1
fruit dry weight [15
Fruit trees, like most trees, use two main sources of N for their vegetative growth and reproduction: the root N uptake and the internal N cycling. The N available for root uptake can derive from mineral fertilizers or from mineralization of native N. Plant roots are able to absorb N in the nitrate (NO3−
) as well as in the ammonium (NH4+
) form, but in well-aerated soils NO3−
is the predominant N source [17
]. Apple trees exposed to NH4+
formed many more flowers than NO3−
-fed trees even when the NH4+
was available for only a very short period [17
]. Throughout the experimental period, NH4+
fertilization led to higher values of the asparagine/arginine ratio in the tree than did NO3−
] demonstrating that asparagine is the main translocation compound for N. Arginine and, to a lesser degree, asparagine, were by far the most abundant levels of the soluble amino compounds in the fertilized trees far above those in the unfertilized trees [17
]. If, and to what extent, the roots of fruit trees are able to absorb organic N (e.g., in the form of aminoacids [18
] is still an open question. Recent evidence suggests that not only ectomycorrhizal fungi, but also arbuscular mycorrhizal associated with tree roots [19
] expand the ability of trees to take up organic N.
After being taken up, the N is translocated through the xylem and allocated to the different organs. Seasonal changes in the amino acidic composition of the xylem sap composition of fruit trees (e.g., apple, cherry, walnut, grape) have been documented and allowed to distinguish between recently root absorbed N and the N deriving from winter storage [19
A considerable amount of the nutrients translocated to the roots can be reloaded into the xylem and translocated back to the shoot, i.e., they are recycled within the plant [20
]. It has been demonstrated for annual plant species that part of the N in the xylem represents a recycled fraction, there are few data for tree species because of the difficulty of measuring this process [21
]. Although the contribution of recycled N to total N flux in the xylem is negligible during the period of spring remobilization of stored N, Grassi et al. [21
] found that it increases exponentially after that period. Grassi et al. [21
] observed in cherry trees that three months after bud burst about 45–50% of total N that passed through xylem was apparently derived from shoot-to-root recycling. They also stated that the recycled N in the xylem was inversely related to total N status of the tree. Therefore, the regulation of N uptake by roots involves shoot-to-root cycling of N: when trees are growing rapidly (e.g., the juvenile and transition phases), or when environmental conditions are more favourable for root activity, there is a high shoot demand for N and a lower proportion of N is translocated back to the roots as aminoacids. On the contrary, when the shoot demand for N is low, there is a relative increase of cycling N in the phloem, which, in turn, depresses further root N uptake.
Reserves throughout woody plants are important for several reasons. Winter survival depends on these adequate reserves. Although regulation of mobilization of root reserves remains unclear, both gibberellins and auxins are possibly involved [22
]. If woody plants use root reserves early in the season, before bud break, most carbohydrates are translocated acropetally within the phloem during the growing season. Phloem loading is an active temperature-dependent process [22
Nitrogen in young tissues, e.g., shoot tips, buds, and new leaves is present mostly as protein [12
]; as new cells are formed, part of the protein N moves from older cells to newer ones, especially when the total N content of the plant is low. Young leaves increase their organic N until they have reached the maturity and full expansion. Under N deficiency, proteins are hydrolyzed (proteolysis) and the resulting aminoacids are distributed to the younger leaves and tips [23
]. The proteolysis results in a collapse of the chloroplasts and a decline of the chlorophyll content. This is the reason why symptoms of N deficiency (yellowish colour) occur first in the older leaves.
N labelled fertilizers have often been used in experiments to elucidate the fate of either the stores N or the fertilizer N. Nitrogen reserves are built up in the previous year and are used to support early growth in the following spring. The contribution of remobilised N to total N needs by trees depends on the tree age and size and the amount of stored N. In deciduous trees (e.g., pear, apple), internal N cycling comprises an intense withdrawal of N from leaves during senescence and its translocation to perennial organs (trunk, old stems, old roots) where they are stored [9
]. In peach trees, for instance, about 50% of leaf N (about 30 kg N ha−1
, according to Niederholzer et al. [24
] is withdrawn before leaf abscission and translocated to storage organs. Roots of fruit trees will store large amounts of N during the winter months and are considered important sources of N in the spring [25
]. Spring N remobilisation from storage organs to developing organs normally precedes root N uptake.
There is a substantial body of literature describing the N uptake and internal cycling of N in deciduous fruit trees, but less information is available for evergreen trees [10
]. In evergreen trees (e.g., citrus), leaves are an important additional sink of N during the winter [10
]. Similarly to deciduous trees, remobilisation of internal N reserves in evergreen trees are crucial for optimal shoot growth, flowering, and fruit set since bud break occurs when conditions (end on winter) are not always optimal for root N uptake [10
]. Once N is absorbed by roots or remobilised from storage reserves, it is allocated to the organs that are developing according to their needs. Shoots, followed by fruits are the main N sinks in orange trees, whose uptake rates in Mediterranean districts in the Northern hemisphere is rather constant from April to November, but relatively less N is partitioned to fruits when the fertilizer N is supplied late in the season [28
]. In several species, there is a low recovery of the labelled fertilizer N in the roots, trunk, and branches that, however, increase their fertilizer N content in winter probably due to the annual N recycling.
4. Soil Management to Enhance Fertilizer Nitrogen Use Efficiency
Enhancing the ability of the soil to support the N nutrition is a key aspect for sustainable N management in orchards; this concept is especially important in organic farming, a type of agriculture that is gaining more and more importance both in terms of cultivated areas and consumers’ acceptance. Most soil N is organic N form and undergoes several chemical and biological transformations whose complete analysis goes beyond the scope of this review.
Several orchard management practices are useful to build-up soil organic N pools, as well as enhance the soil conditions that favour mineralisation. They include (Table 3
) the supply of a large array of organic materials (compost, manure) for both tree nutritional function and to improve soil physical properties, cycling of crop residues (leaves, pruning material), the presence of a natural herbaceous vegetation in the orchard alleys as well as along the tree rows, the use of cover crops, especially those belonging to the Fabaceae family along the tree alleys, subsequently ploughed into the soil.
After its incorporation into the soil, fresh manure releases part of its N quite rapidly, due to the presence of inorganic N (NH4+
), urea, and peptide N fractions. The regular application of manure usually increases the soil organic matter and the activity of the microbial population, as well as the soil aggregation and soil hydraulic properties [43
]. In addition to the environmental conditions, the rate of decomposition of the organic material depends on the quantity and composition of material, like its content on lignin and cellulose, and on the frequency of application [45
]. If carefully managed, losses of N from manure due to leaching, soil erosion, volatilization, and denitrification can be reduced to the minimum.
Mulch has been used in orchards to retain moisture in the soil, suppress weeds and improve the soil fertility. Mulch consists of any type of material spread on the soil surface as a covering. There are several types of organic mulches, including the composted manure and other composted organic materials (bark, straw, senescent leaves). Newly-planted fruit trees under organic farming system should be mulched annually for the first 3–4 years to preserve soil moisture and reduce competition from weeds. Organic mulches have high carbon/nitrogen (C/N) ratio and contain very few available nutrients, including N. For this reason, these organic mulches can trap the residual N present in the soil and prevent its losses.
Cover crops in orchards may also improve plants productivity and simultaneously maintain the ecosystem functioning. Whenever water supply is not limiting, their presence in modern orchards have positive effects on crop yield by suppressing the weeds, controlling the soil erosion, improving the soil quality, and controlling the plant diseases and pests [47
]. Cover crops are usually grasses or legumes, sown or spontaneous, but may include other herbaceous vegetation. Farmers are reluctant to use cover crops in young orchards due to the competition they will establish with the young trees, which may be detrimental to tree growth and future yields. Then, the choice of most suitable cover crop species must be based on well-adapted species to the region taking into account the establishment cost, weed suppression potential, the level of competition with trees, and the ability to improve soil quality. Legumes used as cover crops are important sources of external N, and their use is especially exploited under organic farming. Root nodules infected by rhizobia spp. fix and reduce atmospheric N2
into organic compounds and release it when nodules decompose in the soil. In addition, the residues of legume plants enhance the soil N availability for the main crop, by making some N deriving from the atmosphere available for the decomposition process. An oversupply of N to fruit trees can occur with legume cover crops. However, through proper management practices that suppress the growth and/or decomposition of the legume cover crop (such as mowing or planting non-legumes associated with the legumes to compete with them for N) the N supply to the tree roots will be limited. Symbiotic N2
fixation, however, has rarely been quantified in organically managed orchards. Abscised tree leaves and pruning wood contain significant N amounts. Abscised leaves undergo a series of simultaneous processes of mineralization and immobilization that make N available again for tree root uptake or maintain N in the soil microbial biomass [48
]. These plant residues act as slow-release fertilizers since residues have to be fractionated first, and then mineralized before N is available for plant nutrition. Mineralization rate depends on the amount and composition of senescent leaves and pruning wood material, especially the long C chains, but also the soil type and climatic conditions.
The recycling of N, as a result of the decomposition of senescent leaves in soil was addressed in few studies with apple, peach, and pear trees [48
]. The lifetime of fallen leaves in an orchard and the amount of N returned to the soil are important when analysing the N balance for a sustainable orchard management [48
]. Nitrogen added to the soil by the fallen leaves increases with the amount of abscised leaves, and is affected by tree age and leaf area index (LAI) of trees [48
]. Abscised pear leaves with a C/N ratio of 28 had a decomposition rate (k
) varying from k
= 0.0025 day−1
) to k
= 0.0047 d−1
], while apple leaves with a C/N of 35, after having immobilised some N in the spring following their abscission, decomposed with a k
= 0.0017 d−1
during a period of 102 weeks [50
Pruning wood removed in winter has a high C/N ratio and high lignin content, but contains less N than abscised leaves. If the woody material remains on the soil surface or is incorporated into the soil, it is decomposed very slowly and its N release rate is low and not easy to be predicted. Pruning wood, especially if reduced to small size before soil addition, can trap the residual N present in the soil by the immobilisation process [52
] and prevents the N losses.
5. Efficient Nitrogen Supply Methods
In rain-fed orchards, N should be supplied either before the rainy events or incorporated into the soil by tillage. If mineral fertilizer is used, more than one single dose should be applied along the season. Organic fertilizers can, instead, be applied at a single yearly dose, even in autumn or in winter. Foliar application could also be recommended to complement soil supply whenever trees need N and if it does not rain.
Whenever irrigation water is available, fertigation, i.e., the application of nutrients to fruit trees through the irrigation water, is a valuable tool for providing N whenever it is needed. Fertigation with drip emitters is the most efficient system to simultaneously distribute water and nutrients in small amounts throughout the growth season. This technique has shown good responses on tree growth, yield, and quality, and resulted in a uniform distribution pattern of applied water and N within the active root zone. Several studies have demonstrated a higher N use efficiency when N was supplied by fertigation compared to broadcast applications in apple [53
], citrus [54
], peach [55
], sweet cherry [56
], etc. Nitrogen losses by leaching under fertigation and drip irrigation depends on how water supply is managed: if water supply exceeds the maximum soil water holding capacity, water, and possibly N, is lost by deep percolation; if N is supplied at low rates, the risk of N losses is rather limited.
Foliar nutrient supply is often adopted in fruit trees to complement soil N supply. Fertilizers dissolved in water are sprayed to the aerial organs and absorbed by stomata, aqueous pores and, when the molecule is not-polar, by the cuticle itself. This technique cannot replace the soil N application of fertilizer, but it is a useful tool as particularly summarized in Table 4
. Urea (with low content of biuret <0.3%) is the mostly used and cheapest foliar N fertilizer; due to its not-polar features, it is absorbed rapidly and with high efficiency (up to 90%, [57
]. Suggested rates vary from 0.5% to 2%, but in autumn higher concentration (e.g., 5%) can be applied as well. If compared with soil N supply in late summer/early autumn, foliar urea supply improves tree N reserves without enhancing the risks of causing N losses by leaching. The urea-N that is not absorbed by the spayed leaves is likely to remain on the leaf surface, and when leaves abscise urea-N promotes rapid leaf decomposition on the soil. Dong et al. [59
] found no significant differences in yield and fruit quality between soil and foliar N applications, but soil application increased the NO3−
leaching losses below the root zone, especially late in the growing season of apple trees. In the long run, it might also be risky fully shifting N supply from roots to leaves, as the former need to find adequate N levels in the soil to support their growth.