Context dependent outcomes in a butterfly-ant mutualism: The role of ant nutrition and signaling

Abstract

Food-for-protection mutualisms, interactions between two species in which one species provides protection from aspects of the biotic environment in exchange for a nutritional reward, show an exceptional degree of context dependency. The occurrence, strength, and outcome of these interactions often depend on the ecological context in which they take place. However, the causes and consequences of such context-dependent variation remain poorly understood. The protection mutualism involving lycaenid butterflies and ants provides an opportunity to explore many aspects of the ecology and evolution of interspecific interactions including the importance and predictability of ecological factors that produce context-dependent investment or outcomes in interspecific interactions. Ant-tended lycaenid larvae produce carbohydrate-rich secretions that are collected by attendant ants. In exchange for this food reward, ants may confer developmental benefits and protect larvae from predators and parasitoids. Both participants in this mutualism are capable of responding to changing ecological conditions and, thus, can quickly alter their level of investment or decision to participate in the interaction. In Appendix A, I present the results of field work that illustrate that ant tending provides the lycaenid butterfly, Hemiargus isola, with effective protection from parasitoid attack and enhanced larval survival. Lycaenids on plants from which ants were excluded were almost twice as likely to be parasitized as were lycaenids feeding on plants to which ants had access. In Appendix B, I present the results of laboratory experiments that show that the tentacular organ signal employed by H. isola is a generalized signal, conveyed by either a simple, tactile stimulus or a secretion of low volatility, which evokes an alarm response in attendant ants. Furthermore, I provide evidence to suggest that the function of the tentacular organ signal is context dependent and mediates lycaenid investment in the mutualism. In Appendix C, we present the results of laboratory experiments that demonstrate that altering the ratio of carbohydrate and protein resources available to ants influences their decision to participate in the mutualism with H. isola. Significantly more ants from colonies fed a low carbohydrate/high protein diet tended lycaenids relative to ants fed a high carbohydrate/low protein or high carbohydrate/high protein diet.