Mutualism decline scales up to the community and ecosystem

Background/Question/Methods

Understanding how mutualisms respond to global environmental changes, such as nitrogen (N) deposition, might be important for predicting future community and ecosystem responses. Scaling up of mutualism effects is particularly likely for ecologically-important mutualisms, such as the legume-rhizobium symbiosis, in which traded benefits play a role in structuring the plant community and altering nutrient cycles. In the legume-rhizobium resource mutualism, symbiotic rhizobia provide their legume hosts with fixed N in return for plant photosynthates. Theory predicts that increased resource availability (N) should favor the evolution of less-beneficial rhizobium symbionts. We isolated clover-associated Rhizobium from replicated N-fertilized and control plots in the Kellogg Biological Station LTER and tested these strains in controlled greenhouse experiments to study how 22 years of N fertilization have influenced the evolution and stability of the legume-rhizobium mutualism. Additional mesocosm experiments investigate how evolutionary changes in rhizobia influence plant community composition and N-availability. 

Results/Conclusions

We found that fertilization led to the evolution of rhizobia that are less-beneficial for clover hosts, as evidenced by smaller plants with lower chlorophyll content. Further studies indicate that the strength of this effect (the difference between N- and control-evolved rhizobia) is magnified under carbon-limitation when plants are shaded, suggesting that N-evolved rhizobia alter the cost-benefit ratio of traded benefits for plants. Moreover these effects are not limited to the mutualist partners. In a community mesocosm experiment, inoculation with N-adapted rhizobia shifted plant community composition to favor grasses and forbs, at the expense of clover species, and also caused soil nitrate and ammonium concentrations to decline by 51.6% and 7.7% respectively. The results of several experiments thus suggest that the evolution of mutualism benefits, and ultimately mutualism stability, depend on N fertilization. Moreover these microevolutionary responses scale up to influence ecological interactions in the plant community, shifting the abundance of functional groups, and altering ecosystem processes (soil N-availability). Mutualism evolution might play a surprisingly important role in predicting community and ecosystem responses to global environmental change.