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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...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2018
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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. |
format | Online Article Text |
id | pubmed-6174977 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
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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