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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 ¹⁵ N- and ¹³ C-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 ¹⁵ N and ¹³ C enrichment than adult workers, supporting that the majority of fungal productivity is allocated to colony growth. Foragers assimilated ¹³ C-labeled glucose during its ingestion, but required several days to metabolically process ingested ¹⁵ N-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.

SUBMITTER: Shik JZ

PROVIDER: S-EPMC6174977 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Stable isotope ratios (δ13C and δ15N) have been used extensively to trace nutrients from Pacific salmon, but salmon transfer more than carbon and nitrogen to stream ecosystems, such as phosphorus, minerals, proteins, and lipids. To examine the importance of these nutrients, metrics other than isotopes need to be considered, particularly when so few studies have made direct links between these nutrients and how they affect riparian organisms. Our study specifically examined δ13C and δ15N of riparian organisms from salmon and non-salmon streams in Idaho, USA, at different distances from the streams, and examined whether the quality of riparian plants and the body condition of invertebrates varied with access to these nutrients. Overall, quality and condition metrics did not mirror stable isotope patterns. Most notably, all riparian organisms exhibited elevated δ15N in salmon streams, but also with proximity to both stream types suggesting that both salmon and landscape factors may affect δ15N. The amount of nitrogen incorporated from Pacific salmon was low for all organisms (<20%) and did not correlate with measures of quality or condition, probably due to elevated δ15N at salmon streams reflecting historical salmon runs instead of current contributions. Salmon runs in these Idaho streams have been declining, and associated riparian ecosystems have probably seen about a 90% reduction in salmon-derived nitrogen since the 1950s. In addition, our results support those of other studies that have cautioned that inferences from natural abundance isotope data, particularly in conjunction with mixing models for salmon-derived nutrient percentage estimates, may be confounded by biogeochemical transformations of nitrogen, physiological processes, and even historical legacies of nitrogen sources. Critically, studies should move beyond simply describing isotopic patterns to focusing on the consequences of salmon-derived nutrients by quantifying the condition and fitness of organisms putatively using those resources.

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

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