A Volatile Semiochemical Released by the Fungus Garden of Leaf-Cutting Ants

Sousa, Kátia Kaelly Andrade; Catalani, Gabriela Christal; Gianeti, Thiago Marcelo Ribeiro; Camargo, Roberto da Silva; Caldato, Nádia; Ramos, Vânia Maria; Forti, Luíz Carlos

doi:10.1653/024.103.0401

Cited by 5 publications

(3 citation statements)

References 37 publications

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“…Often, after identifying these allelochemicals, they are used as tools in pest management (36). In the leaf-cutter ant literature as well, the approach has been largely from the direction of behavior to mechanism, and it has been suggested that the cultivar uses volatile semiochemicals to communicate with the ant colony (37) but attempts at identifying these have not been conclusive (38,39). Our approach was different.…”

Section: Lipid Changes Between Fungal Garden and Gongylidiamentioning

confidence: 99%

From plants to ants: Fungal modification of leaf lipids for nutrition and communication in the leaf-cutter ant fungal garden ecosystem

Khadempour

Kyle

Webb-Robertson

et al. 2020

Preprint

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Lipids are essential to all living organisms, as an energy source, as an important cellular structural component, and as a communication tool. In this study, we used global lipidomic methods to evaluate the lipids in leaf-cutter ant fungal gardens. Leaf-cutter ants and their coevolved fungal cultivar, Leucoagaricus gongylophorus, are a model mutualistic system. The fungus enzymatically digests fresh plant material that the ants cut and deliver, converting energy and nutrients from plants, and providing them to the ants through specialized hyphal swellings called gongylidia. Using combined liquid chromatography, ion mobility spectrometry, and tandem mass spectrometry we evaluated differences between the molecular speciation of lipids in the leaf-cutter ant fungal garden ecosystem. This lipidomic study characterized leaves that are fed to the gardens, gongylidia that are produced by the fungus to feed the ants, and spatially resolved regions of the fungal garden through stages of leaf degradation. Lipids containing alpha-linolenic acid (18:3) were enriched in leaves and the top of the gardens, but not dominant in the middle or bottom regions. Gongylidia were dominated by lipids containing linoleic acid (18:2). To evaluate the communicative potential of the lipids in fungal gardens we conducted a behavioral experiment that showed Atta leaf-cutter ants responded differently to 18:3 and 18:2 fatty acids, with aggression towards 18:3 and attraction for 18:2. This work demonstrates the role of lipids in both the transfer of energy and as an inter-kingdom communication tool in leaf-cutter ant fungal gardens.ImportanceIn this work we examined the role of lipids in the mutualism between leaf-cutter ants and fungus. These ants cut fresh leaf material, which they provide to their fungal cultivar, that converts energy and nutrients from the plants and provides it to the ants in specialized hyphal swellings called gongylidia. This work constitutes the first example of a global lipidomics study of a symbiotic system and provides insights as to how the fungus modifies plant lipids into a usable source for the ants. Through a behavioral experiment, this work also demonstrates how lipids can be used as an inter-kingdom communication tool, in this case an attractant, rather than as a repellant, which is more often seen.

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Section: Lipid Changes Between Fungal Garden and Gongylidiamentioning

confidence: 99%

From plants to ants: Fungal modification of leaf lipids for nutrition and communication in the leaf-cutter ant fungal garden ecosystem

Khadempour

Kyle

Webb-Robertson

et al. 2020

Preprint

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“…Often, after identifying these allelochemicals, they are used as tools in pest management ( 36 ). In the leaf-cutter ant literature as well, the approach has been largely from the direction of behavior to mechanism, and it has been suggested that the cultivar uses volatile semiochemicals to communicate with the ant colony ( 37 ), but attempts at identifying these have not been conclusive ( 38 , 39 ). Our approach was different.…”

Section: Discussionmentioning

confidence: 99%

From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem

et al. 2021

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Lipids are essential to all living organisms, as an energy source, as an important cellular structural component, and as a communication tool. In this study, we used global lipidomic methods to evaluate the lipids in leaf-cutter ant fungal gardens. Leaf-cutter ants and their coevolved fungal cultivar, Leucoagaricus gongylophorus, are a model mutualistic system. The fungus enzymatically digests fresh plant material that the ants cut and deliver, converting energy and nutrients from plants and providing them to the ants through specialized hyphal swellings called gongylidia. Using combined liquid chromatography, ion mobility spectrometry, and tandem mass spectrometry, we evaluated differences between the molecular species of lipids in the leaf-cutter ant fungal garden ecosystem. This lipidomic study characterized leaves that are fed to the gardens, gongylidia that are produced by the fungus to feed the ants, and spatially resolved regions of the fungal garden through stages of leaf degradation. Lipids containing alpha-linolenic acid (18:3) were enriched in leaves and the top of the gardens but not dominant in the middle or bottom regions. Gongylidia were dominated by lipids containing linoleic acid (18:2). To evaluate the communicative potential of the lipids in fungal gardens, we conducted a behavioral experiment that showed Atta leaf-cutter ants responded differently to 18:3 and 18:2 fatty acids, with aggression toward 18:3 and attraction for 18:2. This work demonstrates the role of lipids in both the transfer of energy and as an interkingdom communication tool in leaf-cutter ant fungal gardens. IMPORTANCE In this work, we examined the role of lipids in the mutualism between leaf-cutter ants and fungus. These ants cut fresh leaf material, which they provide to their fungal cultivar, that converts energy and nutrients from the plants and provides it to the ants in specialized hyphal swellings called gongylidia. This work constitutes the first example of a global lipidomics study of a symbiotic system and provides insights as to how the fungus modifies plant lipids into a usable source for the ants. Through a behavioral experiment, this work also demonstrates how lipids can be used as an interkingdom communication tool, in this case, as an attractant rather than as a repellant, which is more often seen.

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“…We further tested the hypothesis that the cultivar reinforces optimized nutritional provisioning by signalling its nutritional needs to its ant farmers. Here, we tested two key predictions: (1) the cultivar signals by synthesizing fatty acid compounds with low volatility that provide information at local scales of small garden patches where mulch is deposited (Khadempour et al, 2021;North et al, 1999;Richard et al, 2004;Sousa et al, 2020), and (2) the cultivar concentrates fatty acids in swollen hyphal cells called gongylidia (bundled into staphylae) that are key nutritional rewards consumed by ants (Mueller et al, 2001;Schiøtt & Boomsma, 2021). We then evaluated the fungal cultivar's role in provisioning its ant farmers by tracking the fate of nutrients beyond the initial substrate deposition stage as they travel through leafcutter farming systems.…”

Section: Introductionmentioning

confidence: 99%

Reciprocal nutritional provisioning between leafcutter ants and their fungal cultivar mediates performance of symbiotic farming systems

Bolander,

Andersen,

Conlon

et al. 2023

Functional Ecology

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Optimized food acquisition is challenging because foraged diet items are chemically complex and often nutritionally imbalanced. These challenges are likely magnified when foraged foods are used to provision others (e.g. offspring, nestmates, symbionts) with different nutritional requirements. We used a theoretical framework of nutritional niches to study these provisioning challenges in leafcutter ants that cultivate a fungal symbiont with nutrients derived from freshly foraged plant fragments. While the leaf‐cutting behaviours of free‐ranging foragers are well studied, little is known about how colonies use these plant fragments to produce their fungal crop within underground nest chambers. For instance, gardener ants are known to convert vegetation into a nutritional mulch that they plant on the fungus garden. However, it remains poorly understood how the ants use this mulch to target the specific nutritional needs of their fungal crop, and whether the cultivar signals if provisioned mulch meets its nutritional needs. Towards answers, we performed three experiments to assess the precision and specificity of nutritional regulation in farming systems of the Panamanian leafcutter ant Acromyrmex echinatior. A laboratory feeding experiment with nutritionally defined diets showed that ant farmers collect a specific intake target for protein and carbohydrates and then linked strict protein regulation by foragers to the cultivar's fundamental niche for protein. An in vitro experiment with the fungal cultivar in isolation did not detect a signal of protein stress that could be used by the ants to regulate their provisioning behaviour, but it did identify an elevated fatty acid that may reinforce optimal nutritional provisioning if detected by gardening ants. A feeding experiment with isotopically labelled diets then revealed nutrient‐specific and caste‐specific allocation timelines, with nitrogen being assimilated into the cultivar's nutritional rewards before being exclusively consumed by developing brood. In turn, these combined results help resolve the integrated behaviours that give rise to resilient leafcutter farming productivity. We further show how nutritional niches can help disentangle reciprocal provisioning dynamics between symbionts as well as the nutritional transactions that more generally mediate symbiotic stability (e.g. sanctioning, screening, policing). Read the free Plain Language Summary for this article on the Journal blog.

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A Volatile Semiochemical Released by the Fungus Garden of Leaf-Cutting Ants

Abstract: BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses.

Cited by 5 publications

References 37 publications

From plants to ants: Fungal modification of leaf lipids for nutrition and communication in the leaf-cutter ant fungal garden ecosystem

From plants to ants: Fungal modification of leaf lipids for nutrition and communication in the leaf-cutter ant fungal garden ecosystem

From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem

Reciprocal nutritional provisioning between leafcutter ants and their fungal cultivar mediates performance of symbiotic farming systems

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