Earthworm-enhanced phosphorus availability in soil : from unravelling the mechanisms to assessing its significance

Phosphorus (P) is essential for plant growth, but most of the P in soils is not available for plant uptake as it binds strongly to mineral soil constituents. Additionally, the use of P in agriculture is challenged by both the current increase of the world population as well as a changing human diet towards more consumption of animal products. This results in a growing demand for food and P. Furthermore, the reserves of phosphate rock as source of mineral P fertiliser are declining, while areas that have historically received excessive P additions face environmental risks that are related to chronic dissolved P losses from legacy P soils to ground- and surface waters. These challenges associated with agricultural P use enforce us to increase productivity while using mineral P fertiliser in a more sustainable manner. Sustainable agricultural intensification will require adequate P fertiliser inputs, overcoming global P imbalances and finding ways to improve the utilisation of P already present in soil. This last strategy requires finding new ways to access soil P pools that are less available to plants. Exploring the role of earthworms in sustaining optimal P acquisition for plants can therefore contribute to solving the P challenges we are currently facing. In this thesis, I explored the role of earthworm-enhanced P-availability for improving soil P utilisation. My research primarily focussed on the effect of earthworms in grassland systems from the Netherlands, as grasslands are important to global food production, and can sustain large earthworm populations.The main objective of my thesis was to elucidate the effect of earthworms on plant-available P in soil and P uptake by grass, and to explore its potential to increase the sustainability of P nutrition of grass. The specific research objectives were (1) to assess the effect of different earthworm species on plant-available P and relate this to a) physico-chemical soil properties and b) earthworm ecology; (2) to determine the controlling mechanisms of earthworm-enhanced P-availability and quantify the relative importance of all contributing mechanisms; (3) to assess the effect of earthworm diversity on plant-available P; and (4) to evaluate if the effect of earthworms on plant-available P results in an increased grass P uptake and biomass production under realistic field conditions.My results showed that while all investigated earthworm species increased the total pool of reversibly adsorbed P, a large variation exists in the ability of earthworm species to alter the extent to which P is present in readily plant-available forms. This variation was not related to classical earthworm ecological classification, and species from the same functional group showed large variation in cast properties like pH and dissolved organic carbon as measured in water extracts. In turn, this variation could be linked to the existing variation in ortho-P solubility measured in the same extracts. It was therefore concluded that multiple pathways contributed to earthworm-enhanced P-availability.These multiple pathways were quantified further, and their relative importance was assessed. The probe-ion method, which derives the reactive surface area (RSA) of a soil, in combination with surface complexation modelling revealed a so far unconsidered mechanism: the decrease of the RSA of metal-(hydr)oxides in casts by particle growth, resulting in a decrease of the surface area that is available for P adsorption. The contribution of the controlling mechanisms of earthworm-enhanced P-availability in earthworm casts consists of: a) a relatively small effect of the increase of pH in casts; b) a major contribution of P addition through stimulated mineralisation inside the earthworm gut; c) a potentially major effect of a decrease in the RSA of casts by particle growth which is catalysed by the formation of Fe2+ during the reducing conditions caused by mineralisation; and d) a decrease in the competition between natural organic matter and P for binding sites on metal-(hydr)oxides in casts compared to the bulk soil. The reduction of the RSA was only observed for Fe-(hydr)oxide-dominated soils, whereas it was absent or minor in Al-(hydr)oxide-dominated soils. This demonstrated that soil mineralogy influences earthworm-enhanced P-availability and suggests that earthworms have the largest potential to improve the sustainability of P use in Fe-(hydr)oxide-dominated soils.All controlling mechanisms of earthworm-enhanced P-availability are directly or indirectly related to the capacity of an earthworm to mineralise the organic material it ingests. The potential activity of phosphatase enzymes that catalyse the mineralisation process of monoester P compounds was considerably increased by earthworms in the order casts>burrows>bulk soil. Phosphatase activity varied among earthworm species, and correlated with the P content of grass shoots, suggesting a direct earthworm-induced effect on grass P uptake through mineralisation of organic P.My mesocosm field experiment to the effect of earthworm diversity on grass biomass production and P uptake did not show an effect of a larger number of earthworm species on P uptake at the end of the experiment. However, using a multiple linear regression model on established communities, A. longa and L. terrestris were identified as keystone species to increase grass P uptake and biomass production. Furthermore, this study showed that the effect of earthworms on grass P uptake was not only present under controlled greenhouse conditions but can also be observed at the larger scale of more realistic field conditions.This research concludes that earthworm-enhanced P-availability has potential to contribute to a more sustainable P nutrition for agricultural grasslands in (the future of) the Netherlands. However, the challenges associated with agricultural P use are likely too large to be solved by a single approach. A combination of several approaches is needed by agriculture to provide an adequate P nutrition to grass on low agronomic P-status soils. My research shows that stimulating earthworm populations to increase the utilisation of P in soil could be one of those approaches. Future research should focus on assessing the effect of earthworm-enhanced P-availability on a global scale and its contribution to the utilisation of soil P over longer periods of time. Furthermore, future research should particularly focus on combining earthworms with other approaches that aim to increase P uptake from soils with a low P-status.