Ecology

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Biological damage from water deficit in foragesReports on the tolerance to water deficit damage in the forage cultivars under study are scarce, especially in relation to N and C accumulation, Si effects, and physiological attributes.Pastures grown under water restriction with and without silicon showed a decreased cumulative amount of the beneficial element. However, pastures grown with or without water restriction that had received silicon had an increase in the cumulative amount of silicon (Fig. 2a,d). Carbon content decreased in pastures that had received silicon, regardless of water availability (Fig. 2b,e). Water restriction increased N content in both treatments with and without Si for both forages. Silicon fertigation only in plants with water restriction increased N content in cultivar Massai but decreased it in cultivar BRS Zuri (Fig. 2c,f).Figure 2Silicon (Si) content (a, d), carbon (C) content (b, e) and nitrogen (N) content (c, f) in the aerial part of forage plants cultivated in soil with different soil water retention capacity (WRC) (70 and 40%) absence (− Si) and in the presence of silicon fertigation (+ Si). *Significant to 5% probability by the F test. Lowercase letters show differences in relation to Si and uppercase in relation to WRC. The bars represent the standard error of the mean, n = 6.Full size imageThe present study evidenced, especially with Si addition to the crop, that water deficit in the P. maximum pasture, regardless of cultivar, significantly impairs plant growth by changing homeostasis, i.e., decreasing the C:N ratio by reducing plant C content. This induces instability in the metabolism of the crop, especially in terms of physiological processes31,53. Thus, it was clear that water deficit aggravated physiological stress in the pastures due to an increase in electrolyte leakage, followed by a decrease in Fv/Fm. In other words, photosynthetic efficiency decreased in association with lower relative water content in the plant, which reduced the growth of both P. maximum cultivars.Water deficit in both pastures with and without silicon supply decreased the C:N ratio, except in cultivar Massai, in which the omission of silicon increased this ratio. In an adequate condition of water availability, there was no difference between the absence and presence of Si in the pastures (Fig. 3a,d). Other authors report the same results for different forages, such as sugarcane53. Water deficit in the pastures did not change the C:Si ratio, regardless of Si. In pastures with or without water deficit, silicon fertigation decreased the C:Si ratio (Fig. 3b,e).Figure 3Ratio C:N (a, d), ratio C:Si (b, e) and carbon use efficiency (c, f) in the aerial part of forage plants cultivated in soil with different soil water retention capacities (WRC) (70 and 40%) %) absence (− Si) and in the presence of silicon fertigation (+ Si). *Significant at 5% probability. ns: not significant by the test F. Lowercase letters show differences in relation to Si and capitalization in relation to WRC. The bars represent the standard error of the mean, n = 6.Full size imageAlthough this species has a high capacity for dry matter accumulation because it has a high protein content54, it is sensitive to drought55. Drought damage to plant growth, is due to the loss of stoichiometric stability of nutrients56, which balances the mass of various elements between plants and their environments57.A promising alternative to mitigate water deficit damage in the pasture is the use of Si. This element plays a vital role in the physiological, metabolic, and/or functional processes of plants58 when properly absorbed by the crop. The present study evidences the high capacity of the pastures under study to absorb Si when under water restriction. This is because P. maximum is a Si-accumulating species (leaf Si content > 10 g kg−1), which means that these plants might have specific efficient carriers in the process of Si absorption (monosilicic acid)37,59.Biological benefits of silicon in mitigating water deficit in forageThe high Si absorption by the pastures was important because it was enough to change C and N contents in the pastures under water deficit, and consequently the C:N ratio. However, Si absorption varied depending on the cultivar. In cultivar Massai, the absorption of this element decreased due to an increase in N content, while the opposite occurred in cultivar BRS Zuri. This may have occurred because cultivar Massai has higher N absorption efficiency than BRS Zuri. One cultivar or species may have greater absorption efficiency than another because it has a more efficient nitrogen transporter. In other words, it has better kinetic indexes, such as low KM and minimum concentration, which is governed by genetics31.The decrease in the C:Si ratio in plants grown under water restriction is a result of Si supply, which increased the absorption of this element and decreased C content in both pastures. Long et al.28 also reported the importance of silicon in elementary stoichiometry in a study with banana trees under water deficit.The benefit of stoichiometric homeostasis reflected the high metabolic efficiency of C, that is, Si significantly increased C use efficiency in P. maximum pastures under water restriction (Fig. 3b,e). Other authors report this effect in Brachiaria spp. pastures under drought25 and in sugarcane plants without water stress60.Carbon use efficiency (CUE) decreased in pastures with water restriction without silicon application. However, this variable increased in pastures where this element had been applied. In pastures under adequate water availability, silicon fertigation also increased CUE (Fig. 3c,f). Sugarcane plants under water deficit also showed decreased carbon use efficiency53. This increase in C use efficiency (Fig. 3c,f) by Si may have occurred in both pastures because there was a clear decrease in C content in plants grown under water restriction (Fig. 2b,e).Hao et al.29 reported similar results in native grass species, in which high Si content correlated with low levels of C. This decrease in C content may have occurred because when absorbing the beneficial element, the plant applies an “exchange strategy” to C, particularly in cell wall components such as cellulose. This is because the energy cost of including Si in the carbon chain is lower than that of including C itself61. This strategy thus improves the homeostasis of resistance to water deficiency in pastures. Reports indicate that the increase in Si in plant tissues may decrease lignin synthesis in the cell wall, which has a high energy cost62; The plant uses a “low cost strategy” when occupying binding sites between cell wall components, providing similar structural resistance to that of lignin63.These findings may support the promising role of Si in pasture management. This was evidenced from the effect of Si on elemental stoichiometry homeostasis in both forages grown under water restriction, which favored vital physiological processes by increasing the relative water content of the plant by approximately 14% (Fig. 4a,d). However, the effect of Si on the stoichiometric homeostasis of C might have induced energy savings in the plant, which is critical under water deficit conditions. Plants under water deficit have a limitation in the CO2 assimilation rate accompanied by an increase in the activity of another sink of absorbed energy, for example, photorespiration30. Studies on other crops confirm this finding, indicating a benefit of Si on stoichiometric homeostasis in plants under water deficit. Some examples are the studies of Rocha et al.25 on pasture, and Oliveira Filho et al.26 and Teixeira et al.64 on sugarcane.Figure 4Relative water content (a, d), electrolyte leakage index (b, e) and Total phenolic content (c, f) of forage plants cultivated in soil with different soil water retention capacities (WRC) (70 and 40%) absence (− Si) and in the presence of silicon fertigation (+ Si). *Significant at 5% probability. ns: not significant by the test F. Lowercase letters show differences with respect to Si and uppercase in relation to WRC. The bars represent the standard error of the mean, n = 6.Full size imagePastures under water deficit without silicon fertigation showed decreased relative water content in the plants. On the other hand, silicon fertigation increased the relative water content of forages under water deficit (Fig. 4a,d). Wang et al.65 performed a review to elucidate the effect of silicon on plant water transport processes. The authors indicated that silica deposition on leaf cuticle and stomata decreases water loss from transpiration under water deficit stress. However, accumulating evidence suggest that silicon maintains leaf water content not by reducing water loss, but rather through osmotic adjustments, enhancing water transport and uptake. According to the same authors, enhancement of stem water transport efficiency by silicon is due to silica depositing in the cell wall of vessel tubes, avoiding collapse and embolism.The physiological improvement promoted by Si in attenuating water deficit in pastures probably correlates with the reduction of oxidative stress. In this sense, cell electrolyte leakage decreased (Fig. 4b,e), from the increase of the non-enzymatic antioxidant compound in both forages (Fig. 4c,f) or from the activity of antioxidant enzymes66. This reduces reactive oxygen species, which are common in plants under water deficit67.Water deficiency affected the production of phenolic compounds depending on the cultivar. In Massai, this variable only increased with Si supply; in BRS Zuri, however, it decreased regardless of Si. Plants with silicon fertigation had increased phenolic compound content in pastures under both water availability conditions (Fig. 4c,f). Other authors have reported this effect of Si in increasing phenolic compounds in crops such as faba bean68 and sugar beet69. This supports the hypothesis that Si can attenuate the oxidative stress caused by water deficit by increasing the non-enzymatic antioxidant compound.Exogenous application of Si protects the photosynthetic pigments from oxidative damage by reducing membrane lipid peroxidation. In peanut, this type of application either maintained or reduced H2O268. Another effect of Si that demonstrates the attenuation of oxidative stress in pastures under water deficit was the increase in Fv/Fm; in other words, it favored photosynthetic efficiency. In both pastures, the condition of water restriction without silicon supply decreased the quantum efficiency of PSII (Fv/Fm). However, the supply of silicon in pastures, regardless of water condition, increased the photochemical efficiency of PSII (Fig. 5a,c).Figure 5Quantum efficiency of photosystem II (Fv/Fm) (a, c) and total chlorophyll index (Chl a + b) (b, d) of forage plants grown in soil with different soil water retention capacities (WRC) (70 and 40%) absence (− Si) and in the presence of silicon fertigation (+ Si). *Significant at 5% probability. ns: not significant by the test F. Lowercase letters show differences in relation to Si and capitalization in relation to WRC. The bars represent the standard error of the mean, n = 6.Full size imageThe protection of photosynthetic pigments by Si is also indicative of decreased oxidative stress58. The present study evidenced this situation, as the beneficial element increased the total chlorophyll index in both forages under water deficit (Fig. 5b,d). Wang et al.69 reported that Si delays the degradation of chlorophyll–protein complexes, as the element alters the protein components of the thylakoid, thus optimizing the light collection and stability of PSI. Another benefit of Si would be an increase in osmoprotection as a result of the greater accumulation of metabolites, mainly sugars and sugar alcohols (talose, mannose, fructose, sucrose, cellobiose, trehalose, pinitol, and myo-inositol) and amino acids (glutamic acid, serine, histidine, threonine, tyrosine, valine, isoleucine, and leucine), as seen in peanut plants68.Si benefit on forage productivity under water deficitWater restriction with or without silicon supply decreased the height of both pastures, and silicon application in both water regimes increased plant height (Fig. 6a,d). Water restriction with or without silicon supply decreased the number of tillers in both pastures, except for the cultivar BRS Zuri that had received Si. Silicon application increased the number of tillers in both pastures in both water regimes, except for the cultivar Massai without water restriction (Fig. 6b,e). The dry weight of both pastures decreased under water deficit, regardless of silicon. However, the dry matter of the pastures increased after Si application, with or without water restriction (Fig. 6c,f).Figure 6Plant height (a, d), number of tillers (b, e) and dry matter mass (c, f) of forage plants grown in soil with different soil water retention capacity (WRC) (70 and 40%) absence (− Si) and in the presence of silicon fertigation (+ Si). ns: not significant by the test F. Lowercase letters show differences in relation to Si and capitalization in relation to WRC. The bars represent the standard error of the mean, n = 6.Full size imageThus, the mitigating effects of Si on the physiological processes of both pastures grown under water deficit were responsible for increasing forage growth by promoting an increase of 12% in plant height and 31% in the number of tillers, which is one of the main components of pasture production. This resulted in a 25% increase in dry matter accumulation in relation to the pasture without Si (Fig. 7). Other authors have also reported the mitigating effect of Si on water deficit with a view to increasing plant growth in forage crops70 and other crops like wheat71 and rice72.Figure 7Figure of a forage plant in the condition of water deficit in the absence (− Si) and in the presence of silicon fertigation (+ Si) and a summary of its beneficial in the effects of the plant growth.Full size imageThe present study showed that the effect of Si on the attenuation of drought is not restricted only to physiological aspects involving increased plant water content and photosynthetic or biochemical efficiency. It also regulates elemental stoichiometric homeostasis as discussed above, confirming the biological strategy reported by Hao et al.29 in other forage grasses. Our study indicates that the line of research on the relationship between water deficit and Si in elementary stoichiometry is promising and should advance towards a better understanding of the multiple effects of this beneficial element on the plant.Animal production depends on the amount of biomass produced for grazing. The report of Habermann et al.73 has indicated that climate changes, such as droughts, are threatening pasture production and have a negative impact on animal and protein production. To solve this, the present research serves as a reference for Si fertigation management during the growth of P. maximum. This management consists of a sustainable alternative to improve production with greater nutritional balance even under soil water restriction, favoring water use efficiency in cultivation (Fig. 8). Moreover, Si has long-term potential to reduce the occurrence of droughts, favoring the sustainability of ecosystems. This is because the use of the beneficial element in the soil does not produce greenhouse gases, without negative impacts on the production environment74,75.Figure 8Benefits of Si in elementary stoichiometry and its relationship with physiological and biochemical aspects.Full size imageFuture perspectivesPeatlands and other terrestrial ecosystems represent large reservoirs and filters for Si, controlling Si transfer to the oceans. Land use change during the last 250 years has decreased soil Si availability by increasing export and decreasing Si storage due to higher erosion and a decrease in potentially Si-accumulating plants. Moreover, it has led to a twofold to threefold decrease of the base flow delivery of Si76. This raises concern over forage crops, reinforcing the need for silicate fertilization to explain the response of these species to the application of this element. Future perspectives would focuse on the benefits of Si in elementary stoichiometry and its relationship with physiological and biochemical aspects.Studies should use, other forage species, especially dicotyledons sensitive to water deficit, which have different mechanisms for Si absorption. This will allow a better understanding of whether the Si mechanisms that attenuate drought in monocotyledons also occur in dicotyledons. More

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Crop dataCrop area (in hectare, ha, for sown areas) and production (in kg) statistics on departmental level from 1900 until 1988 were collected from books of national agricultural statistics (‘Statistique agricole annuelle’ or ‘Annuaire de statistique agricole’) compiled by the French Ministry of Agriculture; detailed references are provided in the supplementary information. Numbers were manually digitized from photocopied versions of the original paper documents. Data from 1989 to 2018 were derived from digital statistics from the Agreste database (‘Statistique agricole annuelle’ compiled by the Service de la Statistique et de la Prospective (SSP), Secrétariat Général du Ministère de l’Agriculture, de l’Agroalimentaire et de la Forêt (MAAF), France); details are provided in the supplementary information. Yields were calculated from total production and sown area for each department to avoid apparently often incorrect yield values printed in the old statistics books. Yields are given in kilogram per hectare (kg/ha, for sown area) for dry mass with 10–16% moisture content, depending on the crop.Data are available for ten crops: soft wheat (spring and winter separately), durum wheat, maize, oats (spring and winter), rapeseed (spring and winter), barley (spring and winter), potatoes, sugarbeet, sunflower and wine. The split into spring and winter crops eventually results in 18 distinct crop-cultivar types. Time frames with available data and the correspondence between French and English names are provided in Table 1.Table 1 Data set description for yields on department level.Full size tableThe shapes of French departments have changed over time. We use the 96 mainland (Metropolitan France) departments in their current form and subsume historical values to modern departments as follows. Corsica was one single department until 1975 but then split into Corse-du-Sud and Haute-Corse. Data for Corsica until 1975 were split equally (area, production) or copied (yield) to both new departments. Seine and Seine-et-Oise were two departments until 1967, but then subdivided into seven new departments on 1 January 1968. To account for this, we consider the values of the seven new departments (Essonne, Hauts-de-Seine, Paris, Seine-Saint-Denis, Val-de-Marne, Val-d’Oise, Yvelines) only from 1968 on and unite the two old departments into one counter-factual (“Seine_SeineOise” in the data tables) until 1967.Multiple cropping per year within this set of crops is accounted for by separate area data, but is practically nonexistent in France6.Quality filtersSome yield values had to be considered as outliers, also after checking for digitizing errors. There were four criteria for defining an outlier. First, absolute yield values larger than a physiologically currently unreachable threshold were removed; threshold values were 15 t/ha for barley and durum wheat, 200 t/ha for sugarbeet and potatoes, 20 t/ha for maize, oats and wheat, 10 t/ha for rape and sunflower and 200 hl/ha for wine. These thresholds were chosen to eliminate visually obvious outliers likely due to mismatches between area and production records. The values are set slightly above current maximum attained yields, thus remaining permissive and removing only obvious errors in this first step. Additionally, all yield values for winter rape in 1944, spring rape in 1968 and spring barley in 1980 were removed due to wrongly reported values in the yearbooks. This first step removed in total 167 yield data points. Second, the top 1% of yield values across all departments per decade were removed. Third, values above or below the mean +/− four times the standard deviation of each crop-department time series (for yield, area and production separately) were removed. Fourth, and finally, a similar variance filter as in the third step was applied within each decade of a single time series, filtering values above or below decadal mean +/− two (for yield) or three (area, production) decadal standard deviations. The latter three filters removed, on average, 3.6% of the yield and 0.2% of the area or production data, respectively (Table 1). There were, as a median, 43 yield outliers per department (out of 1,260 data points on average), with a range of 4 (department Hauts de Seine) and 255 (Nord) and an interquartile range of 35–50 outliers. Outliers were masked as missing values to avoid introducing a bias from any correction. In the accompanying data sets we provide two version of the full data set, one without any corrections (“RAW”) and one where the filters described above have been applied (“FILTERED”).ValidationNationally aggregated area, production and yield data from our data set were validated with national data from 1961 to 2018 provided by the FAO (http://faostat3.fao.org/home/E). Area and production data for crops with separate spring and winter data were summed on department level to test agreement with area and production data digitized for the ‘total’ crop. More

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