Foraging trails of leafcutter colonies are iconic scenes in the Neotropics, with ants collecting freshly cut plant fragments to provision a fungal food crop. Leafcutter ants, belonging to the genera Atta and Acromyrmex, exhibit a remarkable symbiotic relationship with a fungus they cultivate for food. These ants don't directly consume the plant matter they collect; instead, they meticulously prepare it as a substrate for their fungal partner, Leucoagaricus gongylophorus. The health and productivity of this fungal crop are directly linked to the nutrients the ants provide, making the leafcutter ant diet a fascinating area of study. This article delves into the intricate dietary needs of leafcutter ants and their cultivated fungus, exploring how these ants navigate the complex nutritional landscape of the rainforest to ensure optimal fungal growth.
The Symbiotic Partnership: Ants and Fungus
The symbiotic relationship between leafcutter ants and their fungus is a prime example of mutualism, where both organisms benefit. The ants provide the fungus with a constant supply of plant material, carefully processed to facilitate fungal growth. In return, the fungus provides the ants with a readily digestible and nutrient-rich food source in the form of gongylidia, specialized fungal hyphal tips.
Nutritional Needs of the Fungus: The Fundamental Nutritional Niche (FNN)
The foundation of the leafcutter ant diet lies in meeting the nutritional requirements of their fungal cultivar, Leucoagaricus gongylophorus. Like all living organisms, the fungus requires a balanced intake of macronutrients (proteins, carbohydrates, and lipids) and micronutrients (minerals and vitamins) for optimal growth and reproduction.
Macronutrient Requirements
Recent laboratory-based experiments with nutritionally defined diets have shown that A. colombica colonies tightly regulate protein foraging at low levels while allowing carbohydrate intake to fluctuate and the cultivar is more sensitive to fluctuations in protein than carbohydrates, with reduced growth and survival when protein concentrations exceed c. 20% total substrate dry mass (Shik et al., 2021). Studies using nutritional geometry (NG) have demonstrated the importance of macronutrient balance in fungal growth. These studies have revealed that Leucoagaricus gongylophorus thrives within a specific range of protein to carbohydrate ratios. The fungus exhibits maximal growth and staphyla density (staphylae are bundles containing gongylidia) when provided with carbohydrate-biased media. Conversely, fungal performance declines when protein-biased provisioning exceeds a certain threshold, around 30%. Staphyla density may exhibit a second FNN peak at elevated protein concentrations (up to 30%) and relatively lower carbohydrate concentrations (up to 20%).
Mineral Requirements
While macronutrients form the bulk of the fungal diet, minerals play a crucial role in various physiological processes, influencing enzyme activity, structural integrity, and overall health. Over 25 mineral elements are essential for life. The effects of mineral composition of plant fragments might influence the suitability of the nutrient blends provided to the fungal culture, thus allowing the cultivar to exploit apparently toxic blends of nutrients. Leafcutter ants concentrate Mg and Ca in their cuticle as a protective armour and Zn as a hardening agent in their mandibles while also preferentially foraging for Na‐rich substrates and avoiding vegetation with elevated Mn and Al.
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Experiments have revealed that certain minerals can significantly impact fungal growth. For example, the minerals P, Al and Fe may expand the leafcutter foraging niche by enhancing the cultivar's tolerance to protein‐biased substrates. A suite of other minerals reduces cultivar performance in ways that may render plant fragments with optimal macronutrient blends unsuitable for provisioning. Three minerals (Al, Fe and P) expanded the fundamental nutritional niche towards elevated growth in protein-rich conditions relative to baseline conditions without these minerals. Seven other tested minerals (Ca, Cu, K, Mg, Mn, Na and Zn) induced varying degrees of toxicity for the cultivar across the gradient of protein and carbohydrate availability
Foraging Strategies: Acquiring the Realized Nutritional Niche (RNN)
Leafcutter ants are selective foragers, carefully choosing plant materials that meet the nutritional needs of their fungus. This foraging behavior is not random; rather, it is a sophisticated strategy aimed at acquiring a realized nutritional niche (RNN) that aligns with the fungus's fundamental nutritional niche (FNN).
Plant Selection
Leafcutter ants forage nutritionally and chemically diverse plant fragments to fit the requirements of their fungal food crop. These ants can select among plant substrates (e.g. leaf, fruit, flower) that have distinct blends of protein, carbohydrates and minerals. Colonies can regulate nutritional intake by foraging across hundreds of plant species to acquire a realized nutritional niche (RNN).
The Role of Plant Chemistry
However, these foraged plant fragments can also contain nutrients in excess of the cultivar's tolerance, which can limit fungal production. The chemical complexity of field-collected vegetation relative to the controlled protein:carbohydrate diets used to assess cultivar's nutritional needs in the laboratory. Plants are typically assumed to contain minerals in sufficient abundance to meet the requirements of insect herbivores, but mineral concentrations vary widely across plant species and tissues within individual plants. Minerals also tend to exhibit thresholds beyond which limitation becomes toxicity and they can even be sequestered by plants to deter herbivores as quantitative chemical defences.
Nutritional Regulation: A Multi-Step Process
Leafcutter ants employ a multi-step process to regulate the nutrition provided to their fungal crop. This process involves:
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- Plant Selection: Ants choose plant materials with specific nutritional profiles, targeting different nutritional blends by foraging among leaves, fruits, flowers, and across plant species. Indeed, a single A. colombica colony can forage across 126 plant species (53 families) and gather up to 370 kg of plant dry mass per year.
- Processing: Gardener ants within underground fungus cultivation chambers macerate vegetation fragments and add a mixture of enzyme‐rich faecal droplets to promote fungal hyphal growth and the production of nutrient-rich hyphal tips called gongylidia.
- Optimization: Colonies forage across plant substrates to acquire a realised nutritional niche (RNN) that targets their cultivar's fundamental nutritional niche (FNN) for maximal crop performance.
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