Biogeochemical cycles in natural forest and conifer plantations in the high mountains of Colombia

Plant litter production and decomposition are two important processes in forest ecosystems, since they provide the main organic matter input to soil and regulate nutrient cycling. With the aim to study these processes, litterfall, standing litter and nutrient return were studied for three years in an oak forest (Quercus humboldtii), pine (Pinus patula) and cypress (Cupressus lusitanica) plantations, located in highlands of the Central Cordillera of Colombia. Evaluation methods included: fine litter collection at fortnightly intervals using litter traps; the litter layer samples at the end of each sampling year and chemical analyses of both litterfall and standing litter. Fine litter fall observed was similar in oak forest (7.5 Mg ha/y) and in pine (7.8 Mg ha/y), but very low in cypress (3.5 Mg ha/y). Litter standing was 1.76, 1.73 and 1.3 Mg ha/y in oak, pine and cypress, respectively. The mean residence time of the standing litter was of 3.3 years for cypress, 2.1 years for pine and 1.8 years for oak forests. In contrast, the total amount of retained elements (N, P, S, Ca, Mg, K, Cu, Fe, Mn and Zn) in the standing litter was higher in pine (115 kg/ha), followed by oak (78 kg/ha) and cypress (24 kg/ha). Oak forests showed the lowest mean residence time of nutrients and the highest nutrients return to the soil as a consequence of a faster decomposition. Thus, a higher nutrient supply to soils from oaks than from tree plantations, seems to be an ecological advantage for recovering and maintaining the main ecosystem functioning features, which needs to be taken into account in restoration programs in this highly degraded Andean mountains.     

大熊猫栖息环境的森林凋落物动态研究

本文以王朗自然保护区冷杉、云杉暗针叶林为对象,在定位测定森林凋落量及其动态和枯枝落叶贮量的基础上,研究了凋落物分解速率及其主要营养元素含量的变化,结果表明：(1)地表枯枝落叶总贮量变化在30.0—91.8t／ha,其中未分解层4.9—17.8,半分解层11.5—19.7,腐殖质层13.6—57.3t／ha。(2)森林凋落的枯枝落叶量因林型不同而略有差异,平均为2.8 t／ha·yr,其凋落高峰期分别在生长季开始的5月和生长季末的10月。(3)每年以凋落物形式返回林地的养分,氮为35.5kg／ha、磷为5.7kg／ha、钾为7.0kg／ha、镁为6.8kg／ha、钙为62.9kg／ha。(4)森林各种凋落物的混合物年分解率为0.3041g／g。95%的凋落物被分解需时约10年,在分解一段时间后,凋落物中的氮、钙、镁含量略有上升,钾明显减少,而磷含量变化不大。(5)森林凋落物的混合物腐解过程中,养分释放速率大小的顺序为：K>P>Mg>Ca>N,大熊猫主食竹的凋落叶则为：K>N>Ca>Mg>P。     

Nutrient dynamics in milpa agriculture and the role of weeds in initial stages of secondary succession in Belize,C.A.

Nutrient levels, soil moisture and soil organic matter were monitored monthly during a three year period in a site cleared for shifting agriculture (milpa) and in adjacement undisturbed high bush forest soils in Belize. Throughout the study there was no evidence of a decline in available nutrient levels in the cleared site. Sharp changes in P and Mn were considered indicative of wetting and drying periods. Corn yields for the rainy season crop in the first two years were average for the region ca 2500 kg ha⁻¹ dry wt, but declined dramatically in the third year. Total weed biomass for the rainy season crop conversely increased every year and reduced grain yield probably through competition for nutrients (especially N), light and water. Substantial amounts of nutrients were also immobilized in the weed biomass, which served the agroecological purpose of preventing nutrient loss by leaching.     

Calcium, potassium, and magnesium cycling in aMexican tropical dry forest ecosystem

We estimated the fluxes, inputs and outputs of Ca, K,and Mg in a Mexican tropical dry forest. The studywas conducted in five contiguous small watersheds(12–28 ha) gauged for long-term ecosystem research. A total of five 80 × 30 m plots were used for thestudy. We quantified inputs from the atmosphere,dissolved and particulate-bound losses, throughfalland litterfall fluxes, and standing crop litter pools. Mean cation inputs for a six-year period were 3.03 kg/ha for Ca, 1.31 kg/ha for K, and 0.80 kg/ha for Mg. Mean outputs in runoff were 5.24, 2.83, and 1.79 kg/ha, respectively. Calcium, K, and Mgconcentrations increased as rainfall moved through thecanopy. Annual Ca return in the litterfall (11.4 g/m²) was much higher than K (2.3 g/m²)and Mg (1.6 g/m²). Litterfall represented 99%of the Ca, 84% of the Mg, and 53% of the K, totalaboveground return to the soil. Calcium concentrationin standing litter (3.87%) was much higher than K(0.38%) and Mg (0.37%). These concentrations werehigher (Ca), lower (K), or similar (Mg) to those inlitterfall. Residence times on the forest floor were0.86, 1.17, and 1.77 yr for K, Mg, and Carespectively. Compared to the residence time fororganic matter at the site (1.31 yr), these resultssuggest slow mineralization for Ca in this ecosystem. Budget estimates were calculated for a wet and a dryyear. Results indicated that nutrients accumulated inthe dry but that nutrients were lost during the wetyear. Comparison of Ca, K, and Mg losses in streamwater with the input rates from the atmosphere for thesix-year period show that inputs are lower thanoutputs in the Chamela tropical dry forestecosystem.     

Controls Over Leaf Litter and Soil Nitrogen Fixation in Two Lowland Tropical Rain Forests

Global comparisons suggest that rates of N fixation in tropical rain forests may be among the highest on earth. However, data supporting this contention are rare, and the factors that regulate N fixation within the biome remain largely unknown. We conducted a full-factorial (N × P) fertilization experiment in two lowland tropical rain forests in Costa Rica to explore the effects of nutrient availability on rates of free-living N fixation in leaf litter and soil. P fertilization significantly increased N fixation rates in both leaf litter and soil, and the effect was dependent on sampling date. Fertilization with N did not affect rates of N fixation at any time. In addition, variation in N fixation rates measured in unfertilized plots at four sampling time points suggested seasonal variability in N fixation: leaf litter N fixation ranged from 0.36 kg/ha/yr in the dry season to 5.48 kg/ha/yr in the wet season. Soil N fixation showed similar patterns ranging from a dry season low of 0.26 kg/ha/yr to a wet season high of 2.71 kg/ha/yr. While the observed temporal variability suggests potential climatic control over free-living N fixation in these forests, data suggest that neither soil nor leaf litter moisture alone regulate N fixation rates. Instead, we hypothesize that a combination of ample C availability, low leaf litter N:P ratios, and high rainfall coincide during the latter portions of the rainy season and drive the highest free-living N fixation rates of the year.     

Litter production,nutrient recycling and litter accumulation inPinus caribaea Morelet var.hondurensis stands in the northern Guniea savanna of Nigeria

Summary The seasonal pattern and quantity of litterfall were studied during a two-year period in two unthinned stands ofPinus caribaea Morelet var. hondurensis Barr. and Golf. in Nigeria. Although pine needles were cast continuously throughout the year, the peak period of litterfall occurred in the dry months of March and April. Mean values of annual litterfall were 3068 and 3665 kg/ha in the two stands aged 7–9 and 9–11 years respectively. Nutrient returns in litterfall in the stands had mean values of 15.0, 0.6, 17.3, 18.2 and 6.3 kg/ha of N, P, K, Ca and Mg respectively. Comparatively low amounts of N and P returned in litterfall were attributed to soil deficiencies of the two elements.Measurements of ground litter showed considerable dry matter accumulation (11378 kg/ha) in the litter layers. Estimates of litter decomposition rate and recycling time showed that it would take 3 to 4 years for the organic matter in annual litterfall to decompose completely as contrasted to about 2 to 5 months often reported under mixed nautral savanna vegetation in the same climatic environment. Similar estimates of nutrient recycling time also showed that between 2 to 4 years were required to mineralize nutrient elements in the annual litterfall; the relative mobilities of the elements were in the order K>Mg>P>NCa.     

Structure and function of shisham forests in central Himalaya,India: nutrient dynamics

The structure and function of Shisham (Dalbergia sissoo Roxb.) forests were investigated in relation to nutrient dynamics in 5- to 15-year-old stands growing in central Himalaya. Nutrient concentrations and storage in different layers of vegetation were in the order: tree > shrub > herb. Forest soil, litter and vegetation accounted for 80.1-91.9, 1.0-1.5 and 7.0-18.4%, respectively, of the total nutrients in the system. There were considerable reductions (trees 32.8-43.1; shrubs 26.2-32.4; and herbs 18-8-22-2%) in nutrient concentrations of leaves during senescence. Nutrient uptake by the vegetation as a whole and also by the different components, with and without adjustment for internal recycling, was investigated. Annual transfer of litter nutrients to the soil from vegetation was 74.8-108.4 kg ha(-1) year(-1) N, 56.8-4 kg ha(-1) year(-1) P and 38.7-46.9 kg ha(-1) year(-1) K. Turnover rate and time for different nutrients ranged between 56 and 66 % year(-1) and 1.5 and 1.8 years, respectively. The turnover rate of litter indicates that over 50% of nutrients in litter on the forest floor are released, which ultimately enhances the productivity of the forest stand. The nutrient use efficiency in Shisham forests ranged from 136 to 143 kg ha(-1) year(-1) for N, 1,441 to 1,570 kg ha(-1) year(-1) for P and 305 to 311 kg ha(-1) year(-1) for K. Compared with natural oak forest (265 kg ha(-1) year(-1) and an exotic eucalypt plantation (18 kg ha(-1) year(-1), a higher proportion of nutrients was retranslocated in Shisham forests, largely because of higher leaf tissue nutrient concentrations. This indicates a lower nutrient use efficiency of Shisham compared with eucalypt and oak. Compartment models for nutrient dynamics have been developed to represent the distribution of nutrients pools and net annual fluxes within the system.     

The Structure and Function of Pine Forest in Central Himalaya. II Nutrient Dynamics

This paper elucidates nutrient dynamics in a pine forest, previouslyinvestigated for dry matter dynamics. The nutrient concentrationsin different life forms were of the order: herb > shrub >tree whereas the standing state of nutrients were of the order:tree > shrub > herb. Soil, litter and vegetation respectivelyaccounted for 38·1–82·2, 2·4–3·7and 15·4–58·2 per cent of the total nutrientsin the system. Considerable reductions (52–69 per cent)in concentrations of nutrient in needles occurred during senescence.The uptake of nutrients by vegetation, and also by differentcomponents with and without adjustment for internal recycling,has been calculated separately. Annual transfer of litter tothe soil by vegetation was 76·21 N, 6·25 P, 57·24Ca, 14·22 Mg, 19·92 K and 1·92 kg ha^–1Na. Turnover rate and turnover time for different nutrientsranged between 0·40–0·64 and 1·56–2·50year, respectively. Compartment models for nutrient dynamicshave been developed to represent the distribution of nutrientcontents and net annual fluxes within the system. Nutrient concentration, standing state, uptake, internal recycling, nutrient return, turnover, nutrient cycling     

Foliar demand and resource economy of nutrients in dry tropical forest species

Important phenological activities in seasonally dry tropical forest species occur within the hot‐dry period when soil water is limiting, while the subsequent wet period is utilized for carbon accumulation. Leaf emergence and leaf area expansion in most of these tree species precedes the rainy season when the weather is very dry and hot and the soil cannot support nutrient uptake by the plants. The nutrient requirement for leaf expansion during the dry summer period, however, is substantial in these species. We tested the hypothesis that the nutrients withdrawn from the senescing leaves support the emergence and expansion of leaves in dry tropical woody species to a significant extent. We examined the leaf traits (with parameters such as leaf life span, leaf nutrient content and retranslocation of nutrients during senescence) in eight selected tree species in northern India. The concentrations of N, P and K declined in the senescing foliage while those of Na and Ca increased. Time series observations on foliar nutrients indicated a substantial amount of nutrient resorption before senescence and a ‘tight nutrient budgeting’. The resorbed N‐mass could potentially support 50 to 100% and 46 to 80% of the leaf growth in terms of area and weight, respectively, across the eight species studied. Corresponding values for P were 29 to 100% and 20 to 91%, for K 29 to 100% and 20 to 57%, for Na 3 to 100% and 1 to 54%, and for Ca 0 to 32% and 0 to 30%. The species differed significantly with respect to their efficiency in nutrient resorption. Such interspecific differences in leaf nutrient economy enhance the conservative utilization of soil nutrients by the dry forest community. This reflects an adaptational strategy of the species growing on seasonally dry, nutrient‐poor soils as they tend to depend more or less on efficient internal cycling and, thus, utilize the retranslocated nutrients for the production of new foliage biomass in summer when the availability of soil moisture and nutrients is severely limited.     

Regional patterns and controls of leaf decomposition in Australian tropical rainforests

Future climates have the potential to alter decomposition rates in tropical forest with implications for carbon emissions, nutrient cycling and retention of standing litter. However, our ability to predict impacts, particularly for seasonally wet forests in the old world, is limited by a paucity of data, a limited understanding of the relative importance of different aspects of climate and the extent to which decomposition rates are constrained by factors other than climate (e.g. soil, vegetation composition). We used the litterbag method to determine leaf litter decay rates at 18 sites distributed throughout the Australian wet tropics bioregion over a 14‐month period. Specifically, we investigated regional controls on litter decay including climate, soil and litter chemical quality. We used both in situ litter collected from litterfall on site and a standardized control leaf litter substrate. The control litter removed the effect of litter chemical quality and the in situ study quantified decomposition specific to the site. Decomposition was generally slower than for other tropical rainforests globally except in our wet and nutrient‐richer sites. This is most likely attributable to the higher latitude, often highly seasonal rainfall and very poor soils in our system. Decomposition rates were best explained by a combination of climate, soil and litter quality. For in situ litter (native to the site) this included: average leaf wetness in the dry season (LWDS; i.e. moisture condensation) and the initial P content of the leaves, or LWDS and initial C. For control litter (no litter quality effect) this included: rainfall seasonality (% dry season days with 0‐mm rainfall), soil P and mean annual temperature. These results suggest that the impact of climate change on decomposition rates within Australian tropical rainforests will be critically dependent on the trajectory of dry season moisture inputs over the coming decades.     

不同季节亚热带常绿阔叶林6个树种凋落叶钙、镁、锰的释放特征

采用凋落物分解袋法,研究了亚热带常绿阔叶林区马尾松、柳杉、杉木、香樟、红椿、麻栎6个典型树种凋落叶的Ca、Mg、Mn在第一个分解年不同雨热季节的释放特征.结果表明：经历1年的分解,6种凋落叶Ca、Mg、Mn释放率分别为-13.8%～92.3%、4.0%～64.8%和41.6%～81.1%.马尾松和香樟凋落叶Ca释放动态呈现富集-释放模式,其余4种凋落叶整体上呈现释放的模式;香樟凋落叶Mg释放动态呈现富集-释放模式,其余5种凋落叶呈现直接释放模式;柳杉和红椿凋落叶Mn释放动态呈现富集-释放模式,其余4种凋落叶呈现直接释放模式.凋落叶Ca、Mg、Mn的释放明显受到季节性降雨的影响,且因凋落叶种类不同而有差异.Ca、Mg、Mn在雨季的释放率和释放量均高于旱季.初始养分含量和降雨量是影响凋落物分解过程元素释放的重要因子.     

Litter production and forest floor nutrient dynamics in pine and hardwood stands of New Brunswick, Canada

Biomass and nutrient transfer (N, P, K, Ca, Mg) of overstory (branches and leaves) and understory litter fall were examined over a two year period in four jack pine stands aged 16, 29, 49 and 57 years and four mixed hardwood stands aged 7, 17, 20 and 29 years. Relative amounts of the five nutrients in litter fall for both series of stands were N > K ≷ Ca > P = Mg. Return of mineral elements to the forest floor was generally twice as high on the hardwood stands as for similarly aged pine stands. Overall return of nutrients plotted versus stand age generally exhibited a plateau relationship, with relatively little difference among stands; however, some exceptions occurred. Understory contribution to litter fall was very important on these stands, since in most cases the nutrient mass in understory litter was usually similar to or higher than that from the tree layer. Data on forest floor biomass, nutrient distribution and turnover rates of these stands were also presented; mobility of nutrients in the forest floor was in the order K > Mg ≥ P ≥ Ca ≥ N.     

兴安落叶松人工林营养元素的分析

落叶松人工林能否保持无机动态平衡、稳定生长,主要取决于每年还原于土壤中凋落物营养元素成分和数量。本研究目的在于揭示凋落物变化的各种规律,以及营养元素的潜在还原量。为改善林地条件,建立最佳结构模式的林分提供科学依据。为此我们对黑龙江省东部尚志县帽儿山兴安落叶松人工林四年凋落物营养元素进行了分析研究。结果表明: 1.落叶松树种的凋落物数量,包括叶、枝、皮等,四年平均每公顷干重量为3099.5kg,林内天然阔叶树为237.4kg,总计为3336.9kg。 2.不同种类凋落物营养元素的含量差异显著,叶含量最多,枝次之,皮中含量最小。 3.平均每年每公顷还原于林地的营养元素总量(N、P、K、Ca、Mg、Cu、Zn、Mn)为98.8697kg,其中落叶松叶为85.5998kg,阔叶树叶为8.385kg,落叶松落枝为2.0335kg,林内落叶松落皮为9.13kg,阔叶树枝为9.27kg。     

天然枫桦红松林凋落量动态及养分归还量

三年定位研究表明小兴安岭天然枫桦红松林年均凋落量有5.8t／ha(干重)。凋落量的季节变化格局是随着气候变冷有一明显秋季凋落高峰期(9—10月)。凋落物每年养分的归还量：Ca、N、K、Mg、P,相应为67.0、56.9、14.8、9.5、和6.6kg／ha,总计155.0kg／ha。据测定阔叶树落叶养分含量明显高于所有针叶的含量。尽管阔叶树的年凋落量仅占该混交林的年总凋落量的三分之一,阔叶树落叶仍有相当高的养分比例(43.4%)归还土壤。因此,红松林分的经营管理中,保留适当比重的阔叶树有利于土壤改良和促进林分生长。     

Variation in Canopy Litterfall Along a Precipitation and Soil Fertility Gradient in a Panamanian Lower Montane Forest

Fertilization experiments in tropical forests have shown that litterfall increases in response to the addition of one or more soil nutrients. However, the relationship between soil nutrient availability and litterfall is poorly defined along natural soil fertility gradients, especially in tropical montane forests. Here, we measured litterfall for two years in five lower montane 1‐ha plots spanning a soil fertility and precipitation gradient in lower montane forest at Fortuna, Panama. Litterfall was also measured in a concurrent nitrogen fertilization experiment at one site. Repeated‐measures ANOVA was used to test for site (or treatment), year, and season effects on vegetative, reproductive and total litterfall. We predicted that total litterfall, and the ratio of reproductive to leaf litterfall, would increase with nutrient availability along the fertility gradient, and in response to nitrogen addition. We found that total annual litterfall varied substantially among 1‐ha plots (4.78 Mg/ha/yr to 7.96 Mg/ha/yr), and all but the most aseasonal plot showed significant seasonality in litterfall. However, litterfall accumulation did not track soil nutrient availability; instead forest growing on relatively infertile soil, but dominated by an ectomycorrhizal tree species, had the highest total litterfall accumulation. In the fertilization plots, significantly more total litter fell in nitrogen addition relative to control plots, but this increase in response to nitrogen (13%) was small compared to variation observed among 1‐ha plots. These results suggest that while litterfall at Fortuna is nutrient‐limited, compositional and functional turnover along the fertility gradient obscure any direct relationship between soil resource availability and canopy productivity.     

Distribution and budget of nutrients in a commercial apple orchard

Summary Data on the dry matter distribution and nutrient reserves (N, P, S, Cl, K, Ca, Mg and Na) in the standing biomass of a grassed-down 14 year-old apple orchard are presented together with mean estimates of nutrient inputs, returns and losses over a 2 year period.The major inputs of N P K and S were through fertilizer additions. The major inputs of Na and Cl were in bulk precipitation plus irrigation whilst both sources were important for Mg and Ca. Total inputs by precipitation plus irrigation plus fertilizer in kg/ha/yr were: N, 81; P, 20; S, 42; Cl, 58; K, 64; Ca, 35; Mg, 10 and Na, 33. Nutrient returns to the orchard floor were dominated by those from returns of herbage clippings orginating from the mowing of the orchard pasture. Autumn leaf fall also contributed significant quantities to the total nutrient returns. Total nutrient returns to the orchard floor through petal fall, fruit drop, leaf fall, foliar leaching (includes leaf washing) and pasture clippings in kg/ha/yr were: N, 545; P, 33; S, 41; Cl, 107; K, 442; Ca, 147; Mg, 35 and Na, 16. The major loss of Na, Mg, Ca, Cl and S was through leaching (this may include a certain amount of chemical weathering). In contrast, the major loss of P and K was in the harvested fruit crop, while for N, losses were about equally divided between the fruit crop and leaching. Total nutrient losses from the orchard by removal of the fruit crop and pruning wood plus leaching losses were estimated in kg/ha/yr at: N, 58; P, 5; S, 28; Cl, 81; K, 124; Ca, 55; Mg, 39 and Na, 80. Inputs minus losses in kg/ha/yr were positive for N, P and S(+23, +16 and +14 respectively and negative for Cl, K, Ca, Mg and Na (–24, –60, –19, –30 and –47 respectively).     

Temporal patterns of soil nutrients in a Panamanian moist forest revealed by ion-exchange resin and experimental irrigation

The effect of seasonal water availability on soil nutrients and soil N transformations was investigated by irrigating two large plots of mature tropical forest on Barro Colorado Island (BCI), Panama, during the dry season for five consecutive years. Methods included (i) nutrient accumulation by ion-exchange resins placed on the surface of the mineral soil for contiguous 21-day periods, (ii) monthly mineral soil (0–10 cm) extractions and incubations for inorganic N and P concentrations, and (iii) leaching loss of nutrients from leaf litter samples. Rates of nutrient accumulation by the resins showed a great deal of variation between sampling dates and among years in control plots; albeit, seasonal patterns were slight, except for the highest Ca values near the end of the wet season and inorganic P (P_i) and SO₄ values that peaked during the dry season. Irrigation had remarkably little effect on nutrient accumulation rates by resins, except for an increase in Mg and Na values, but did affect the timing in the temporal variation in K, Na, N_i and P_i values. In contrast, inorganic N (N_i) and P_i pools and N transformation rates in the mineral soil hardly varied among sampling dates and did not show any response to irrigation. We hypothesize that the timing of leaf litterfall and nutrient leaching from forest floor litter can set up temporal patterns in the levels of soil nutrient at the surface of the mineral soil, but the temporal patterns essentially disappear with depth in the mineral soil.     

Under-storey Nutrient Content in an Age Sequence of Douglas-fir Stands

The nutrient concentrations and contents of the under-storeyspecies were estimated for a series of Pacific North-west Douglas-fir[Pseudotsuga menxiessii (Mirb.) Franco] stands ranging in agefrom 9 to 95 years. Analyses were carried out for ash, N, P,K, Ca, Mg, Mn, Fe, Zn and Na and significant differences innutrient concentrations were found to exist between species;species rejecting certain nutrients and accumulating others.General trends for mean concentrations of some nutrients areassociated with stand maturity in that ash, K and Mg decline,P and Mn increase and N and Ca reaches a peak at 20–30years and then declines. The nutrient contents (kg ha^–1)of the under-storey component of the stands are presented andtrends discussed. Mineral nutrient content, under-storey vegetation, Pseudotsuga menziessii stands, Douglas-fir     

西藏色季拉山暗针叶林凋落物层化学性质研究

The storage and chemical properties of the forest litter in dark coniferous forest of Sejila Mountain were studied. The results showed that the existing storage was 5. 863t·hm^-2 and the annual litter fall was 0. 3205 t·hm^-2 It implied that the forest litter decomposed slowly and accumulated quickly, and the turnover of nutrient circles was slow. The contents of N, Ca, Na, and Mn nutrient elements in litter layer were in the order of un-decomposed layer (U layer) > semi-decomposed layer (S layer) > decomposed layer (D layer), those of K, Fe, and Mg were in the order of D layer > S layer > U layer, and P element content was in the order of U layer > D layer> S layer. The pool of elements was 78. 483 kg·hm^-2 N, 3. 843 kg·hm^-2P, 48. 205 kg·hm^-2 K, 23.115 kg·hm^-2 Ca, 13. 157 kg·hm^-2 Na, 30.554 kg·hm^-2 Fe, 2. 113 kg·hm^-2 Mn and 27. 513 kg·hm^-2 Mg. The turnover of forest litter was the total of nutrient release accumulation. K, Fe, and Mg were enriched, and N,Ca, Na, Mn, and P were released with the turnover rate in the order of N > Ca > Na > Mn >P.