TY - JOUR

T1 - Reciprocal nutritional provisioning between leafcutter ants and their fungal cultivar mediates performance of symbiotic farming systems

AU - Bolander, Mille

AU - Andersen, Julie Elmegaard

AU - Conlon, Benjamin H.

AU - Arnan, Xavier

AU - Michelsen, Anders

AU - Shik, Jonathan Zvi

N1 - Publisher Copyright: © 2023 The Authors. Functional Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.

PY - 2023

Y1 - 2023

N2 - 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.

AB - 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.

KW - leafcutter ants

KW - Leucoagaricus gongylophorus

KW - nutritional geometry

KW - stable isotopes

KW - symbiosis

U2 - 10.1111/1365-2435.14437

DO - 10.1111/1365-2435.14437

M3 - Journal article

AN - SCOPUS:85172026347

VL - 37

SP - 3079

EP - 3090

JO - Functional Ecology

JF - Functional Ecology

SN - 0269-8463

IS - 12

ER -