The high cost of mutualism: effects of four species of East African ant symbionts on their myrmecophyte host tree

Background/Question/Methods

Three recent meta-analyses of protective plant-ant mutualisms report a surprisingly weak relationship between herbivore protection and measured demographic benefits to ant-plants, suggesting high tolerance for herbivory, substantial costs of ant-mediated defense, and/or benefits that are realized episodically rather than continuously. Experimental manipulations of protective ant-plant associations typically last for less than a year, yet virtually all specialized myrmecophytes are long-lived perennials for which the costs and benefits of maintaining ant symbionts could accrue at different rates over the host’s lifetime. To complement long-term monitoring studies, we experimentally  excluded each of four ant symbionts from their long-lived myrmecophyte host trees (Acacia drepanolobium) for 4.5 years. 

Results/Conclusions

Ant species varied in their effectiveness against herbivores and in their effects on intermediate-term growth and reproduction, but the level of herbivore protection provided was a poor predictor of the net impact they had on host trees.  Removal of the three Crematogaster species resulted in cumulative gains in host tree growth and/or reproduction over the course of the experiment, despite the fact that two of those species significantly reduce chronic herbivore damage. In contrast, although T. penzigi is a relatively poor defender, the low cost of maintaining this ant symbiont apparently eliminated negative impacts on overall tree growth and reproduction, resulting in enhanced allocation to new branch growth by the final census. Acacia drepanolobium is evidently highly tolerant of herbivory by insects and small browsers, and the costs of maintaining Crematogaster colonies exceeded the benefits received during the study. No experimental trees were killed by elephants, but elephant damage was uniquely associated with reduced tree growth, and at least one ant species (C. mimosae) strongly deterred elephant browsing. We hypothesize that rare but catastrophic damage by elephants may be more important than chronic herbivory in maintaining the costly myrmecophyte habit in this system.