The interaction effect of soil organisms and plant intraspecific diversity on ecosystem functions

Plant diversity and soil organisms are both widely studied for their contributions to ecosystem functions. It has been recently shown that soil biota may drive the plant species diversity-function relationship in grasslands, while so far studies on plant intraspecific diversity are lacking. To improve the understanding of how ecosystem functions may be influenced by plant intraspecific diversity, soil organisms, and their interactions, we used a field setting to examine the effects of plant intraspecific diversity and functionally dissimilar soil organisms (manipulated by the addition of plant-parasitic nematodes, earthworms, and arbuscular mycorrhizal fungi) on aboveground primary production, pollination and shoot herbivory. Plant intraspecific diversity was manipulated by sowing different seed mixtures of Trifolium pratense L. and Lolium perenne L. cultivars. We found a positive effect of plant intraspecific diversity on total aboveground biomass, contributed mostly by T. pratense. The plant intraspecific diversity-productivity effect on T. pratense was mediated by plant-parasitic nematodes, i.e. aboveground biomass was increased by intraspecific diversity only in the nematode treatment. Further, the average floral visitation length was decreased by earthworm addition, while the abundance of pollinators tended to be increased by high plant intraspecific diversity. Aboveground biomass of L. perenne and leaf damage of T. pratense were not influenced by the treatments. We conclude that plant intraspecific diversity and soil organisms can interactively or independently modify functions such as aboveground primary production and pollination of T. pratense in the field. Specifically, the positive plant intraspecific diversity effect appears to only emerge under conditions of stress (high nematode abundance). This result indicates that plant intraspecific diversity may be important for the maintenance of ecosystem functions, especially in an agricultural context, where pest pressure can be high and can have large detrimental consequences. Introduction Changes in plant species diversity have been reported to affect ecosystem functions and processes, such as plant productivity, vegetation dynamics and insect food web interactions (Hector et al. 1999, Cardinale et al. 2011, Tilman et al. 2012). Previous studies have shown that the effect of plant species diversity on aboveground primary production can be modified by soil organisms, such as arbuscular mycorrhizal fungi (AMF) or plant pathogens (van der Heijden et al. 2008, Schnitzer et al. 2010, Maron et al. 2011, Eisenhauer et al. 2012a). While numerous biodiversity-ecosystem functions studies have focused on plant species diversity (Hooper and Vitousek 1997, Grime 1998, The effect of AMF, earthworms, nematodes and plant intraspecific diversity 43 Hector et al. 1999, Loreau and Hector 2001), increasing attention has been paid to the possible consequences of plant genotypic diversity for ecosystem functions (Zhu et al. 2000a, Crutsinger et al. 2006, Crawford and Rudgers 2012, Tooker and Frank 2012, Shoffner and Tooker 2013). Some recent studies have indicated a comparable importance and similar influence of genotypic diversity and plant species diversity for increasing plant productivity (Crutsinger et al. 2006, Cook-Patton et al. 2011, Roger et al. 2012). Changes in plant intraspecific diversity have been shown to influence not only plant productivity (Himanen et al. 2013), but also community stability (Prieto et al. 2015), stress tolerance, and the resistance of plant community to herbivores and plant invaders (Kotowska et al. 2010, Tooker and Frank 2012, Yang et al. 2012, Shoffner and Tooker 2013). In previous studies, the positive effect of plant intraspecific diversity on plant productivity was usually explained by two main processes, the selection effect and the complementary effect (Hughes et al. 2008, Cook-Patton et al. 2011, Tooker and Frank 2012). First, high intraspecific diversity plots have greater odds of containing more productive and pathogen resistant cultivars (selection effect) (Fox 2005, Tooker and Frank 2012). Second, complementary traits and functions of cultivars may result in increased plant productivity (complementary effect) (Loreau and Hector 2001, Poisot et al. 2013). Besides the effects on plant productivity, it has been proposed that plant intraspecific diversity may have effects on soil biota communities, albeit sometimes idiosyncratic ones (Cadet et al. 2006, Crutsinger et al. 2008b). For example, intraspecific genetic structure and community composition of soil microorganisms have been reported to be influenced by plant genotypes (Schweitzer et al. 2008, Gehring et al. 2013) or by plant cultivars (Dalmastri et al. 1999, Inceoglu et al. 2010). However, the role of soil biota in modifying the impact of plant genotypic diversity on ecosystem functions is not well understood. Previous studies show that aboveground ecosystems in general can be influenced by soil biota in a variety of ways (Clay and Holah 1999, Klironomos 2002, Wardle et al. 2004). The effect of soil organisms on plant performance ranges from beneficial to detrimental (Wagg et al. 2011, Bardgett and van der Putten 2014). Functionally dissimilar soil organism groups are widely known to be of prime importance for soil processes such as organic matter turnover, nutrient cycling and uptake, and engineering of soil physical properties (Wurst et al. 2012). Earthworms, for example, the most recognized soil engineering organisms, can modify soil structure and enhance the availability of soil nutrients for plants through burrowing, casting and bioturbation (Edwards and Bohlen 1996). AMF can improve plant uptake of nutrients (mainly phosphorous) by forming a network of fine extra-radical hyphae (Smith and Read 2008). Plant-parasitic nematodes, known as pest organisms in agriculture, can inhibit plant growth through their direct root feeding; yet, they can also indirectly increase nutrient mineralization through increased carbon and nutrient leaching from the