The multidimensional nutritional niche of fungus-cultivar provisioning in free-ranging colonies of a neotropical leafcutter ant

Abstract

The foraging trails of Atta leafcutter colonies are among the most iconic scenes in Neotropical ecosystems, with thousands of ants carrying freshly cut plant fragments back to their nests where they are used to provision a fungal food crop. We tested a hypothesis that the fungal cultivars multidimensional requirements for macronutrients (protein and carbohydrates) and minerals (Al, Ca, Cu, Fe, K, Mg, Mn, Na, P and Zn) govern the foraging breadth of Atta colombica leafcutter ants in a Panamanian rainforest. Analyses of freshly cut plant fragments carried by leafcutter foragers showed that the combination of fruits, flowers, and leaves provide for a broad realized nutritional niche that can maximize cultivars performance. And, while the leaves that comprised the most harvested resource also delivered an intake target containing protein in excess of the amounts that can maximize cultivar growth, in vitro experiments showed that the minerals P, Al, and Fe can enhance the cultivars tolerance to protein-biased substrates, and potentially expand the ants foraging niche. Yet, the cultivar also exhibits narrow margins between mineral limitation and toxicity that may render plant fragments with seemingly optimal blends of macronutrients unsuitable for provisioning. Our approach highlights that optimal foraging is inherently multidimensional and links the foraging behavior of a generalist insect herbivore to the fundamental nutritional niche of its microbial symbiont. Significance StatementColonies of Atta colombica leafcutter ants can contain millions of specialized workers exhibiting large-scale generalist herbivory. Yet, this generalist foraging niche also depends on the poorly understood physiological needs of the ants domesticated fungal cultivar. We show the cultivars fundamental nutritional niche is broad for carbohydrates but narrower for protein and a suite of minerals, but that the cultivars sensitivity to excess protein is also mediated by Al, Fe, and P. More generally, this study decouples the multidimensional foraging strategies that enable a generalist herbivore to navigate a complex nutritional landscape and mix many imbalanced foods to achieve balanced cultivar provisioning.