P for Two, Sharing a Scarce Resource: Soil Phosphorus Acquisition in the Rhizosphere of Intercropped Species

Abstract

Over the last 50 years, the use of nitrogen (N) and phosphorus (P) fertilizers has increased at a faster rate than global food production, resulting in substantial decreases of N and P efficiency in agriculture (Fig. 1). Thus, considerable amounts of N and P fertilizers have been wasted in agroecosystems, and the alteration of N and P biogeochemical cycles is among the most visible impacts of human activities on ecosystem services, far exceeding the hypothesized “planetary boundaries” for N and approaching those for P (Rockström et al., 2009). Projections for the future suggest that a substantial further increase in N and P fertilizer use will occur to cope with increasing food demand (Tilman et al., 2001; Vance et al., 2003). Tilman et al. (2001) predicted that global consumption of fertilizer P will increase from 34.3 Tg year−1 in 2000 to a mean projected value of 83.7 Tg year−1 in 2050 (56.2–118 Tg year−1 depending on the calculation scenario). Such increases in fertilizer consumption will further threaten the global N and P cycles. Bouwman et al. (2009) estimated that in 2000, the total input of fertilizer P in croplands amounted to 21 Tg year−1, of which 9 Tg was accumulated in soils and 1 Tg was lost to erosion. Their projections for 2050 for various scenarios of future agricultural development amounted to 29 to 46 Tg year−1 total P fertilizer input and 10 to 23 and 3 to 5 Tg year−1 accumulated in soil and lost to erosion, respectively. This suggests that even in the most optimistic scenario, the contribution of P fertilization of cropland to P movement by erosion will triple over the period 2000 to 2050. While further intensification of agroecosystems is clearly needed to cover the growing food demand over the next decades, we cannot afford to accept the “business as usual” scenario that relies on ever-increasing agricultural inputs and the resulting waste of nutrients in some regions of the world (Vitousek et al., 2009). Relative increase in world annual production of cereals, and global annual consumption of fertilizer N and fertilizer P over the period from 1961 to 2008. The 100-basis in 1961 corresponds to 876.9 Tg cereals year–1, 11.6 Tg fertilizer N year–1, and 4.8 Tg fertilizer P year–1. In 2008, these values were 2,520.7 Tg cereals year–1, 101.6 Tg fertilizer N year–1, and 17.1 Tg fertilizer P year–1. (Data are from FAOSTAT [http://faostat.fao.org/], accessed February 20, 2011). Contrary to N, P is reasonably abundant in the Earth’s crust (1.2 g kg–1 on average) and thus in soils, where it primarily occurs as inorganic P in apatite minerals derived from the bedrock. However, with soil formation and weathering, total P content decreases over time and organic P content builds up at the expense of inorganic P, as shown in soil chronosequences (Richardson et al., 2004). At early stages of development (in young soils), therefore, terrestrial ecosystems are primarily N limited, while at later stages of development (in older soils), they become P limited (Vitousek and Farrington, 1997). Thus, soil P scarcity is especially critical in the tropics, where deeply weathered soils dominate. In addition, unlike N (especially nitrate), phosphate ions are poorly mobile and present at low concentration in soil solution, due to strong and multiple interactions with soil constituents (Hinsinger, 2001). These comprise adsorption onto soil minerals (metal oxides and clay minerals), precipitation as P minerals (predominantly apatite-like minerals), and immobilization as various organic P compounds (soil organic matter and phytate, which is the P storage form in seeds). P limitation is thus widespread, estimated to affect about 5.7 billion ha worldwide (Gaume, 2000). While, in spite of their considerable energy cost, the reservoir of atmospheric N2 used for manufacturing N fertilizers is much larger than required, the situation for P is rather different. World reserves of P ores are indeed finite, and the exact time when their consumption will peak is a matter for debate. High-grade phosphate rocks are definitely expected to be exhausted within the next decades (Cordell et al., 2009), which calls into question the sustainability of current P fertilizer use in developed and emerging countries. Increasing P efficiency in crops without further increasing P inputs requires better exploration and exploitation of soil resources in agroecosystems. To achieve this, we must breed more P-efficient crop genotypes that will make better use of belowground (root architecture and rhizosphere-related) traits (Vance et al., 2003; Lynch, 2007). Another promising option for achieving ecological intensification of agroecosystems (Cassman, 1999) is to make better use of plant diversity, especially niche complementarity and facilitation occurring in the rhizospheres of intercropped species (Zhang et al., 2010). Enhanced productivity of multispecies agroecosystems (intercropping) compared with that of monospecific agroecosystems (each of