Disentangling nutritional pathways linking leafcutter ants and their co‐evolved fungal symbionts using stable isotopes

Abstract

Leafcutter ants are the ultimate insect superorganisms, with up to millions of physiologically specialized workers cooperating to cut and transport vegetation and then convert it into compost used to cultivate co‐evolved fungi, domesticated over millions of years. We tested hypotheses about the nutrient‐processing dynamics governing this functional integration, tracing 15N‐ and 13C‐enriched substrates through colonies of the leafcutter ant Atta colombica. Our results highlight striking performance efficiencies, including rapid conversion (within 2 d) of harvested nutrients into edible fungal tissue (swollen hyphal tips called gongylidia) in the center of fungus gardens, while also highlighting that much of each colony's foraging effort resulted in substrate placed directly in the trash. We also find nutrient‐specific processing dynamics both within and across layers of the fungus garden, and in ant consumers. Larvae exhibited higher overall levels of 15N and 13C enrichment than adult workers, supporting that the majority of fungal productivity is allocated to colony growth. Foragers assimilated 13C‐labeled glucose during its ingestion, but required several days to metabolically process ingested 15N‐labeled ammonium nitrate. This processing timeline helps resolve a 40‐yr old hypothesis, that foragers (but apparently not gardeners or larvae) bypass their fungal crops to directly assimilate some of the nutrients they ingest outside the nest. Tracing these nutritional pathways with stable isotopes helps visualize how physiological integration within symbiotic networks gives rise to the ecologically dominant herbivory of leafcutter ants in habitats ranging from Argentina to the southern United States.

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

“…On the other hand, the ant's digestive system has adapted to prevent digestion of fungus-produced plant biomass degradation enzymes so that the ants can redistribute them through fecal fluid onto freshly incorporated leaf material (21). In return, the fungus provides all of the nutrients to feed the colony by producing carbohydrate, polysaccharide, and lipid rich gongylidia (24,25).…”

Reconstructing the functions of endosymbiotic Mollicutes in fungus-growing ants

“…Tissues of adult insects no longer grow and may thus only need small amounts of nitrogen for maintenance, so passing on excess NH 3 to fungus gardens via fecal fluid would have unambiguous benefits for the complex mutualism as a whole ( Schiøtt et al, 2010 ). This conjecture was recently confirmed for Atta workers in an independent study showing that workers fed with ammonium nitrate (the protonated form of ammonia) transfer nitrogen via their fecal fluid to the fungus garden ( Shik et al, 2018 ). Mollicutes-assisted garden manuring would thus imply that any surplus nitrogen remains a stable resource for new fungal protein synthesis and thus growth of the ant brood that only ingests fungal food.…”

“…The evolutionarily derived attine lineages rear fully domesticated and co-adapted fungal cultivars that provide the ant farmers with specialized hyphal tips (gongylidia) containing mostly carbohydrates and lipids that the workers harvest and digest ( De Fine Licht et al, 2014 ; Quinlan and Cherrett, 1979 ). The ant brood is completely dependent on the ingestion of fungal biomass ( Hölldobler and Wilson, 1990 ), but workers may ingest and assimilate liquids as well ( Littledyke and Cherrett, 1976 ; Shik et al, 2018 ). However, similar to other ants, they cannot ingest solid plant or animal fragments that they collect to provision their fungus gardens because a sieve in the infrabuccal cavity filters out any particles in excess of ca.…”

Using Nutritional Geometry to Explore How Social Insects Navigate Nutritional Landscapes

“…At least four species of Lasius cover their 'carton' nests with a mycelial coat, with L. fuliginosus using a Cladosporium, and L. umbratus likely cultivating Hormiscium pithyophilum [56]. Using fluorescently dyed fungal hyphae [57] and stable isotope enrichment experiments (e.g., heavy forms of carbon, 13 C and nitrogen, 15 N) [58] the speed and targeted nature of nutrient exchange between ants and their fungal mutualists can be shown. This bidirectional nutritional mutualism is an ideal study system for the application of NG tools.…”

“…Each farming colony cultivates a single fungal crop in monoculture [60] by harvesting resources ranging from detritus to fresh vegetation [61]. The ants convert these otherwise inedible substrates into nutritional mulches used to provision their fungi that in turn is consumed as their primary food source [34,58]. The Atta and Acromyrmex leafcutter ants display the highest degree of partner specialization, using mostly freshly cut vegetation to provision a Leucoagaricus gongylophorus cultivar that produces swollen hyphal tips called gongylidia that concentrate nutrients [62].…”