Phosphorus mobilization in low-P arable soils may involve soil organic C depletion
Graphical abstract
Introduction
Phosphorus (P) is the second most limiting nutrient for crops, after nitrogen (N) (Vance et al., 2000). Crop yield is limited by P availability in about 40% of the world's arable land mainly in highly weathered, acidic or calcareous soils (Krämer and Green, 2000, Sánchez and Salinas, 1981). Thus, since the green revolution, considerable amounts of P fertilizer have been used in agricultural lands in order to increase and maintain high crop production (Tilman, 1999, Tilman et al., 2002). Most P fertilizers are obtained from mining activities and are thus considered a nonrenewable resource (Childers et al., 2011). P sources are nowadays being depleted, resulting in a need to identify farming systems capable of increasing P use efficiency while maintaining high yields. Low input farming systems are one option for increasing nutrient use efficiencies, as in some cases they have been proven to maintain high productivity (de Ponti et al., 2012) by increasing soil nutrient stocks while reducing inputs of nonrenewable resources (Stockdale et al., 2001). The use of legumes and organic fertilizers are likely the main farming practices that contribute to the buildup of nutrient reserves in these agronomic systems (Watson et al., 2002). However, in many cases low input farming systems show low soil retained P pools and availability in the long term (Wivstad et al., 2005, Romanyà and Rovira, 2009, Ryan and Kirkegaard, 2012) that may have implications on crop yield and on the cycling of other nutrients, such as N or even on soil organic matter.
Phosphorous availability is especially relevant to legume crops which have particularly high P requirements due to the high demand of P for biological nitrogen fixation (Smith, 1992). This is especially the case in systems aimed at maximizing nitrogen fixation (Sulieman et al., 2013) such as low input farming systems. In consequence, low P availability can limit both crop growth and biological nitrogen fixation (Almeida et al., 2000, Reed et al., 2007, Smith, 1992). P fertilization can increase P availability despite most of the added P becoming unavailable to plants due to soil adsorption, precipitation with Fe, Al and Ca and its retention in the organic matter pool (Gichangi et al., 2009, Romanyà and Rovira, 2009).
Soil P can occur in organic and inorganic forms. These forms can be strongly retained in soils (retained P) or can be readily mobilized (soluble P). Organic P transformation in soils remains poorly understood in comparison to inorganic P (Turner et al., 2013). Organic P can be transformed to inorganic via mineralization by root or microbial-released phosphatases (Chang et al., 2007) or can be immobilized in organic forms mainly through microbial processes (Hansen et al., 2004). Plant residues can also contribute to soil organic P; indeed, the most abundant soil organic P form (phytate) can originate from plant material (Selle et al., 2000). Crops can only use organic P after mineralization (Adams and Pate, 1992). Organic P mineralization is regulated by the extracellular presence of soil phosphatases that are produced mainly by soil microbiota, although plants can also exude acid phosphatases (George et al., 2011). Indeed, acid phosphatase production is closely tied to root growth and activity (Dinkelaker and Marschner, 1992, Krämer and Green, 2000) while alkaline phosphatase has not been detected in plants (Juma and Tabatabai, 1988, Tarafdar and Jungk, 1987). The activity of these extracellular enzymes can be linked to soil microbial and/or root activity and to P requirements of soil biota (Nannipieri et al., 2011). It is known that the application of inorganic P inhibits phosphatase activity (Olander and Vitousek, 2000), while this inhibition has not been found after applying organic fertilizers (Kremer and Li, 2003). On the other hand, plants and soil microbiota can also contribute to increasing soil P solubility by excreting low molecular weight organic acids into the rhizosphere and by lowering the soil pH in the case of alkaline soils (Gerke and Meyer, 1995, Nahas et al., 1990). The release of organic acids has been found to destabilize soil organic matter from organo-mineral complexes and thus prime decomposition (Clarholm et al., 2015, Keiluweit et al., 2010). Soil organic matter may enhance P desorption and mobility by enhancing soil microbial activity and by reducing soil P sorption capacity (Ayaga et al., 2006, Iramuremye and Dick, 1996). High stabilization of organic P on soil binding sites that occur in low organic matter soils may depress P mineralization as soil microbiota may not have access to soil organic P (Romanyà and Rovira, 2007). Indeed, several authors have observed increased microbial activity after adding P in P-limited soils (Cleveland and Townsend, 2006, Nottingham et al., 2015). In contrast, other studies have shown that P mineralization can be driven by the microbial need for carbon (C) (Heuck et al., 2015, Spohn and Kuzyakov, 2013, Wang et al., 2016) and thus microbial P mineralization can be a side effect of microbial C acquisition from which plants can potentially benefit. On the other hand, plants can contribute to organic matter mobilization on the search of P and to its subsequent mineralization by soil microbiota (Clarholm et al., 2015). Thus, the stoichiometry of C and P may be affected by plant-microbiota P demand and by the C requirements of microbiota.
Within this context, we investigated the release of soil retained inorganic and organic P pools that took place under two legume crops grown on soils with contrasting fertility, as well as tested the effects of applying manure. The release of P retained in mineral and organic pools during one crop period depend on the plant-microbiota capacity to mobilize P by exuding organic acids and phosphatase enzymes and on the availability of soil retained P and organic C in the soil environment. In low-P soils, P may be strongly retained mostly in organo-metal complexes while in high-P soils it may be less strongly retained in such bonding sites and may be thus readily mobilized. We hypothesize that in low-P soils roots and soil biota will mobilize organic C from organo-metal complexes on the search of P at a greater rate than in high P soils.
Our aims were: (1) to study the changes in soil retained P pools occurring during the growth of two legume crops in two contrasting P availability scenarios, (2) to relate the changes in soluble P forms with the changes occurring in the soil retained P and organic C during legume crop growth, and (3) to provide insight on the mechanisms of soil retained P mobilization during the growth of legume crops in high- and low-P soils.
Section snippets
Site and treatments
The study area consisted of two arable fields with contrasting P availability located in the peri-urban rural area of Gallecs, Catalonia (low-P field; 41° 33′ 37″ N, 2° 11′ 37″ and high-P field; 41° 33′ 49″ N, 2° 12′ 07″ E). At sampling time, these fields had been organically managed for three years following European regulations (EC 834/2007). The climate is dry sub-humid Mediterranean with a mean annual temperature of 15.5 °C and mean annual rainfall of 602 mm. Soils are loams and described
Soluble inorganic and organic P forms
At sowing time, soluble Pi was much higher in the high-P field than in the low-P field (p < 0.001) and showed large increases after adding manure in both fields (Fig. 1a and b). In unfertilized soils, soluble Pi increased in the late flowering stage, while it decreased only in the low-P field fertilized soils. Soluble Po showed a very different behavior; at the time of sowing it was highest in the low-P field (p < 0.001) and did not show any effect of fertilization. At the late flowering stage,
Phosphorus availability
Based on P standards for rain-fed fields, soluble Pi levels in the low-P field are very low, while in the high-P field they are clearly in the very high range, more than 30 mg P kg−1 (Yanez, 1989). We took advantage of this large difference between the two nearby fields to attempt to explain the variations in P pools and C stocks observed during a period of legume growth. Despite showing a great range of productivity (from 60 to 3000 kg ha−1), the effects of both legume species on soil P pools
Conclusions
During crop growth, plants and soil microbes mobilize large amounts of retained Pi that are mostly transformed into retained Po. In low-P soils, both retained Po and soluble Po contributed to soluble Pi by mineralization processes likely mediated by acid phosphatase activity. Microbial mobilization of retained Po that takes place under conditions of P starvation may deplete organic C. In contrast, in high-P soils, P transformations appear to be less organic C demanding. Thus, low-P availability
Acknowledgements
We wish to thank Miriam Burriel and Damaris Cardona for help in the field and in the lab, and to an anonymous referee for constructive comments on the manuscript. We also wish to thank Salvi Safont for help in setting up the experimental layout and Alicia Speratti for editing English. This research was supported by the FERTILCROP project (www.fertilcrop.net) funded by CORE Organic Plus Funding Bodies, partners of the ERA-Net (www.coreorganic2.org) and Lindeco (CGL2009-13497-CO2-02), as well as
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