Selection for protection in an ant-plant mutualism: host sanctions, host modularity and the principal-agent game

Retaliation against cheaters can prevent the breakdown of cooperation. Here we ask whether the ant-plant Cordia nodosa is able to apply retaliatory sanctions against its ant symbiont Allomerus octoarticulatus, which patrols new shoots to prevent herbivory. We test the hypothesis that the modular design of C. nodosa physiologically ties the growth of housing (stem swellings known as domatia) to the successful development of the attached leaves. We experimentally simulated herbivory by cutting leaves from patrolled shoots and found that the domatia on such 'cheated' shoots suffered higher mortality and lower growth than did controls, evidence for a host sanction. On the other hand, patrolling is costly to the ant, and experiment shows that non-patrollers run a low risk of being sanctioned because most leaves (and the attached domatia) escape heavy herbivory even when patrollers are absent. This suggests that cheaters might enjoy a higher fitness than do mutualists, despite sanctions, but we find that patrolling provides a net fecundity benefit when the colony and plant exceed a minimum size, which requires sustained ant investment in patrolling. These results map directly onto the principal-agent (P-A) game from economics, which we suggest can be used as a framework for studying stability in mutualisms, where high sampling costs and cheating do not allow market effects to select for mutual benefits.