Soil Fertility Increases with Plant Species Diversity in a Long-Term Biodiversity Experiment

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Soil Fertility Increases with Plant Species Diversity in a Long-Term Biodiversity Experiment Oecologia DOI 10.1007/s00442-008-1123-x ECOSYSTEM ECOLOGY - ORIGINAL PAPER Soil fertility increases with plant species diversity in a long-term biodiversity experiment Ray Dybzinski · Joseph E. Fargione · Donald R. Zak · Dario Fornara · David Tilman Received: 18 January 2008 / Accepted: 21 July 2008 © Springer-Verlag 2008 Abstract Most explanations for the positive eVect of than seedlings grown in soil collected beneath monocul- plant species diversity on productivity have focused on the tures. This increase was likely attributable to greater soil N eYciency of resource use, implicitly assuming that resource availability, which had increased in higher diversity com- supply is constant. To test this assumption, we grew seed- munities over the 10-year-duration of the experiment. In a lings of Echinacea purpurea in soil collected beneath distinction akin to the selection/complementarity partition 10-year-old, experimental plant communities containing one, commonly made in studies of diversity and productivity, two, four, eight, or 16 native grassland species. The results we further determined whether the additive eVects of func- of this greenhouse bioassay challenge the assumption of tional groups or the interactive eVects of functional groups constant resource supply; we found that bioassay seedlings explained the increase in fertility with diversity. The grown in soil collected from experimental communities increase in bioassay seedling biomass with diversity was containing 16 plant species produced 70% more biomass largely explained by a concomitant increase in N-Wxer, C4 grass, forb, and C3 grass biomass with diversity, suggesting that the additive eVects of these four functional groups at Communicated by Louis Pitelka. higher diversity contributed to enhance N availability and retention. Nevertheless, diversity still explained a signiW- R. Dybzinski · D. Fornara · D. Tilman cant amount of the residual variation in bioassay seedling Department of Ecology, Evolution, and Behavior, biomass after functional group biomass was included in a University of Minnesota, St Paul, MN 55108, USA multiple regression, suggesting that interactions also J. E. Fargione increased fertility in diverse communities. Our results sug- Midwest Resource OYce, The Nature Conservancy, gest a mechanism, the fertility eVect, by which increased Minneapolis, MN 55415, USA plant species diversity may increase community productiv- D. R. Zak ity over time by increasing the supply of nutrients via both School of Natural Resources and Environment, greater inputs and greater retention. University of Michigan, Ann Arbor, MI 48109, USA Keywords Cedar Creek · Sampling eVect · Legume D. R. Zak Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, USA Introduction D. Fornara Institute of Environmental and Natural Sciences, V Lancaster University, Lancaster LA1 4YQ, UK Many researchers have found a positive e ect of plant spe- cies number (hereafter “diversity”) on productivity Present Address: (reviewed in Hooper et al. 2005; Kinzig et al. 2002; Loreau R. Dybzinski (&) et al. 2002; Spehn et al. 2005), and most explanations for Princeton Environmental Institute, Princeton University, V Princeton, NJ 08544, USA this e ect have focused on either the greater presence of e-mail: [email protected] productive species or greater complementarity in the modes 123 Oecologia and timing of resource consumption in diverse communi- soil beneath high-diversity plant communities had greater ties (Huston 1997; Loreau and Hector 2001; Tilman et al. microbial biomass and respiration than low-diversity com- 1997b, 2001). However, an additional mechanistic distinc- munities, largely due to increased plant biomass (and hence tion can be made between the eVect of diversity on resource litter) in the high-diversity communities (Zak et al. 2003). consumption and on resource supply. A positive eVect of However, increased plant biomass could not completely diversity on resource supply, (i.e., a “fertility eVect”), might explain an increase in N mineralization associated with be expected to amplify the observed positive eVect of diver- higher diversity communities (Zak et al. 2003), indicating sity on plant productivity through time, and, like eVects of that plant diversity increases mineralization rates, and diversity on resource consumption, may be driven by the hence soil fertility, by mechanisms beyond those associated greater likelihood of including particular traits at higher with increased biomass. Moreover, they and others have diversity, the greater likelihood of interactions between par- demonstrated that higher diversity communities in the same ticular traits at higher diversity, or a combination of these. experiment have more N in plant pools than lower diversity However, there is limited evidence for increased soil fertil- communities, consistent with the idea that soil fertility ity beneath species-rich plant communities (Balvanera et al. increases with plant diversity (Fargione et al. 2007; Zak 2006; Zak et al. 2003) because most biodiversity experi- et al. 2003). ments have not been conducted long enough for such an Here, using data from the same long-term Weld experi- eVect to manifest. ment, we: (1) test for a “fertility eVect”—the positive eVect Composition and diversity may aVect fertility through of plant diversity on soil fertility (Zak et al. 2003)—using diVerential species eVects on nutrient inputs. Plants that additional measures of fertility; and (2) determine whether form associations with N-Wxing bacteria (hereafter “N-Wxers”) the additive eVects of species traits (“additive fertility may increase soil N availability. Like every functional eVects”), the interaction of species traits (“interactive fertil- group, N-Wxers are more likely to be present in diverse ity eVects”), or both are responsible. Because plant growth communities (Huston 1997; Spehn et al. 2002; Tilman et al. is an integrated measure of soil nutrient availability, we 2001). Diverse plots may also promote microbial communi- used a seedling bioassay to assess how plant diversity inXu- ties that mineralize a larger fraction of recalcitrant organic ences the fertility of soil beneath species-poor and species- N (Zak et al. 2003), eVectively increasing inputs of this rich plant communities. In addition, we include total soil N growth-limiting nutrient, or they may support or attract and N mineralization as additional measures of soil fertility greater consumer biomass and thus receive higher levels of in our analyses. labile inputs through frass or feces. The mechanisms aVecting productivity across diversity Composition and diversity may also aVect fertility gradients are now routinely partitioned into selection and through diVerential species eVects on nutrient retention. complementarity eVects (e.g., Lanta and Leps 2007; Polley Importantly, the high root biomass of some grasses and the et al. 2007; Spehn et al. 2005). Unfortunately, it is not pos- overall greater average root biomass of diverse plots may sible to partition the eVects on soil fertility in the same way promote the retention of N by preventing leaching because, unlike a species’ biomass in mixture, a species’ (Scherer-Lorenzen et al. 2003; Tilman et al. 1996). Addi- contribution to soil fertility in mixture cannot be directly tionally, interspeciWc diVerences may interact to reduce measured. Nevertheless, we present an analysis in the spirit nutrient losses, such that diverse communities retain more of the selection/complementarity distinction by ascribing nutrients. For example, species diVer in their phenology, fertility eVects to the additive eVect of species traits (analo- ¡ + V depth, and form (e.g., NO3 vs. NH4 ) of nutrient uptake gous to selection) and the interactive e ect of species traits (McKane et al. 1990, 2002) such that diverse plots are (analogous to complementarity). expected to more completely capture nutrients through time We based our test on the assumptions that: (1) additive and space and across diVerent nutrient forms. Other inter- and interactive eVects completely explain the overall eVect speciWc diVerences may aVect soil fertility: for instance, of diversity on soil fertility, and (2) the additive eVect of a diVerences in stoichiometry (Reich and Oleksyn 2004) may functional group on soil fertility is linearly related to its aVect rates of nutrient recycling (Wedin and Tilman 1990), biomass. It follows from these two assumptions that inter- and the eVects of specialized enemies and mutualists (Bar- active eVects on soil fertility would be revealed by signiW- telt-Ryser et al. 2005; Klironomos 2003; Knops et al. 1999; cant eVects of diversity after statistically controlling for Mitchell et al. 2002) may indirectly aVect nutrient inputs or functional group biomass. For example, both N-Wxer bio- retention by aVecting species composition. mass and C4 grass biomass increased with diversity in our In a long-term biodiversity experiment established on experiment due to overyielding and their greater likelihood low-N, sandy soil, Zak et al. (2003) demonstrated that some of being included in higher diversity plots (see “Results” of the microbial processes that aVect resource supply were and Fargione et al. 2007). If N-Wxer biomass and N reten- positively aVected by plant species diversity. For example, tion from C4 grasses were the only factors that aVected soil 123 Oecologia fertility, then the greater fertility of diverse plots would be the experiment was seeded), 2004,
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