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

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 nutr...

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Autores principales: Shik, Jonathan Z., Rytter, Winnie, Arnan, Xavier, Michelsen, Anders
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6174977/
https://www.ncbi.nlm.nih.gov/pubmed/30067862
http://dx.doi.org/10.1002/ecy.2431
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author Shik, Jonathan Z.
Rytter, Winnie
Arnan, Xavier
Michelsen, Anders
author_facet Shik, Jonathan Z.
Rytter, Winnie
Arnan, Xavier
Michelsen, Anders
author_sort Shik, Jonathan Z.
collection PubMed
description 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.
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spelling pubmed-61749772018-10-15 Disentangling nutritional pathways linking leafcutter ants and their co‐evolved fungal symbionts using stable isotopes Shik, Jonathan Z. Rytter, Winnie Arnan, Xavier Michelsen, Anders Ecology Articles 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. John Wiley and Sons Inc. 2018-08-01 2018-09 /pmc/articles/PMC6174977/ /pubmed/30067862 http://dx.doi.org/10.1002/ecy.2431 Text en © 2018 The Authors Ecology published by Wiley Periodicals, Inc. on behalf of Ecological Society of America. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Articles
Shik, Jonathan Z.
Rytter, Winnie
Arnan, Xavier
Michelsen, Anders
Disentangling nutritional pathways linking leafcutter ants and their co‐evolved fungal symbionts using stable isotopes
title Disentangling nutritional pathways linking leafcutter ants and their co‐evolved fungal symbionts using stable isotopes
title_full Disentangling nutritional pathways linking leafcutter ants and their co‐evolved fungal symbionts using stable isotopes
title_fullStr Disentangling nutritional pathways linking leafcutter ants and their co‐evolved fungal symbionts using stable isotopes
title_full_unstemmed Disentangling nutritional pathways linking leafcutter ants and their co‐evolved fungal symbionts using stable isotopes
title_short Disentangling nutritional pathways linking leafcutter ants and their co‐evolved fungal symbionts using stable isotopes
title_sort disentangling nutritional pathways linking leafcutter ants and their co‐evolved fungal symbionts using stable isotopes
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6174977/
https://www.ncbi.nlm.nih.gov/pubmed/30067862
http://dx.doi.org/10.1002/ecy.2431
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