Discussion
Our competition experiment in a common garden shows that early-season differences in species’ growth rates in monoculture are good predictors of short-term differences in relative abundance in pairwise and five species mixtures and that predictions were stronger under productive (light-limited) conditions. The species that grew faster early in the season (i.e. H. lanatus and A. pratensis) , had the greatest competitive advantage relative to slower-growing species (i.e.A. odoratum , A. elatius and F. rubra ). Relative differences in species growth rates became smaller as the growing season progressed until they eventually became negatively associated with differences in species biomass. This switch corresponds to the time at which faster growing species had already reached their maximum growth rate and gradually slowed down while the RGR of slow-growing species was still rising (around day 134 in the year – 13/05/2008). Early differences in species’ growth rate also governed short-term competitive outcomes in our semi-natural grassland subjected to nutrient addition, thereby extending the results of the common garden experiment to a real-world grassland ecosystem. Together these results indicate that species growing faster during the early stage of the growing season, and thus reducing light availability during this early phase of vegetation growth, had a competitive advantage relative to species that initially grow more slowly.
Addition of nitrogen in our semi-natural grassland ecosystem increased productivity and reduced plant diversity, allowing us to further assess whether differences in species growth rate predict short-term competitive exclusion due to nutrient addition. We found that difference in early season RGR predict short-term competitive exclusion under productive conditions, but not under unproductive conditions. Under productive conditions, the species that grew faster early in the season (e.g. Anemonetrullifolia,Gentiana sino-ornata, andSaussurea nigrescens) , competitively excluded initially slower growing species (e.g. Potentillaanserina, Potentillafragarioides, Euphorbiaaltotibetica and Geraniumpylzowianum ). This result suggests that when nutrient limitation is alleviated and productivity is increased, the resulting decline in diversity is partly caused by species that grow fast initially reducing resource availability and outcompeting species that grow more slowly.
Previous studies have shown that under productive conditions, when competition is mainly for light, asymmetric competition causes plant species intercepting more light early in the season to have a disproportionate advantage, leading to competitive exclusion of subordinate species (HautierVojtech et al., 2018, Vojtech et al., 2008, Vojtech et al., 2007, Hautier, 2009, DeMalach et al., 2017). Our study is the first to our knowledge to reveal the critical time during the growing season when exclusion mechanisms act. We show that differences in early season growth rates (day 53 when the growing season starts at ~ day 106 in Zurich and around day 155 when the growing season starts at ~ day 136 in Gansu) provide an explanation of competitive outcomes, thereby serving as a predictor and early signalling of plant competitive abilities. This is because under productive conditions, asymmetric competition leads to increased relative size differences between species early in the season. This early advantage allows fast-growing species to maintain and increase their initial dominant position throughout the growing season, leading to the exclusion of initially slower growing species. Our study is in agreement with earlier studies demonstrating that instantaneous measurements of light obtained early in the season, at the critical time when light becomes limiting for plant growth, were the best predictors of competitive outcomes (Vojtech et al., 2007, Violle et al., 2007).
Our results from the field experiment are based on a subset of the total number of species occurring in the community. Growth rates were derived from the twenty most common species across all treatments, accounting for 85 ± 10% of the total aboveground biomass. Our results are therefore most likely conservative because they are restricted to competitive exclusion amongst the twenty-most common species, thereby failing to consider the exclusion of the rarest species, which comprise a large proportion of the total species number and are more susceptible to human disturbances.
Previous studies have shown that the outcome of competition in pairwise mixtures could be best predicted by differences in light intercepting ability in monocultures (I* ) under productive (light-limited) conditions and by differences in nutrient uptake ability in monocultures (R* ) under unproductive conditions (Dybzinski and Tilman, 2007, Vojtech et al., 2007, HautierVojtech et al., 2018). However, in real-world ecosystems that encompass nutrient gradients, both forms of competition are likely to act at the same time, with light competition becoming more important as nutrient competition lessens. Our results are consistent with the resource ratio hypothesis envisaging a trade-off between competition for light under fertile conditions and for nutrients under less fertile conditions. Under fertile conditions, species growing faster early in the season have a competitive advantage over initially slower-growing species (consistent with them being better competitors for light). This relationship between RGR and competitive success weakens under less fertile conditions (compare fertile conditions with added nitrogen from less fertile conditions without added nitrogen in Figures 1, 2 S3, S5 and S6). However, we would expect, based on earlier work (Tilman and Wedin 1991, Wedin and Tilman 1993), that slow-growing species with the lowest R * for soil resources would dominate the community in the long-term (a long-term outcome that we were not able to assess in our relatively short-term study). This would require that slow growing species do not entirely disappear from the landscape.
Our study thus suggests that human activities that increase the availability of nutrients to ecosystems will likely further reduce plant diversity in the future by benefitting initially fast-growing species. In contrast, management practices directed towards reducing the growth of fast-growing species early in the season should help efforts to protect and restore biodiversity in an increasingly human-dominated world. For example, parasitic plants such as Rhinanthus species can restore biodiversity in productive grasslands (DiGiovanni et al., 2017, Bardgett et al., 2006, Pywell et al., 2004, Bullock and Pywell, 2005). A potential mechanism is through the reduction of the biomass of competitively dominant grasses (Davies et al., 1997, Ameloot et al., 2005), simply because the parasite reduces host resources leading to a reduction in host growth rate and future resource uptake (Hautier et al., 2010). Our results suggest that Rhinanthus species could be particularly effective because they cancel out the initial advantage of fast-growing species early in the season thus limiting the exclusion of slower-growing species. Adjusting the timing and frequency of cutting could also be used as a restoration tool in nutrient-rich grasslands. For example, a higher frequency of cutting that alters the structure of the canopy layer can reduce asymmetric competition for light and the initial advantage of fast growing species, giving slow growing species more equal chances to compete for the limiting resources (HautierVojtech et al., 2018, Talle et al., 2018). On the other hand, multiple cuts per season may reduce the number of flowering plant and seeds that impact pollination, food for plant-feeding insects, seed recruitment and nesting sites for birds (Plantureux et al., 2005). Our results suggest that an early cut combined with a late cut in the season could constitute a good management strategy. While an early cut reduces competition for light and the competitive dominance of fast-growing species, thus promoting diversity, a late cut provides nesting sites and allows plants to produce flowers and mature seeds. Additionally, cutting with subsequent haying has the advantage of removing plant biomass and excess accumulated nutrients in the soils, allowing the subsequent recovery of diversity (Storkey et al., 2015). Alternatively, low-diversity stable state could persist even after decades of cessation of nutrient enrichment if biomass is not removed and recycled within the system (Tilman and Isbell, 2015, Isbell et al., 2013).