Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched With Biologically Important Elements
Fungus-farming within galleries in the xylem of trees has evolved independently in at least twelve lineages of weevils (Curculionidae: Scolytinae, Platypodinae) and one lineage of ship-timber beetles (Lymexylidae). Jointly these are termed ambrosia beetles because they actively cultivate nutritional...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-04-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.664542/full |
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| author | Maximilian Lehenberger Maximilian Lehenberger Nina Foh Axel Göttlein Diana Six Peter H. W. Biedermann Peter H. W. Biedermann |
| author_facet | Maximilian Lehenberger Maximilian Lehenberger Nina Foh Axel Göttlein Diana Six Peter H. W. Biedermann Peter H. W. Biedermann |
| author_sort | Maximilian Lehenberger |
| collection | DOAJ |
| description | Fungus-farming within galleries in the xylem of trees has evolved independently in at least twelve lineages of weevils (Curculionidae: Scolytinae, Platypodinae) and one lineage of ship-timber beetles (Lymexylidae). Jointly these are termed ambrosia beetles because they actively cultivate nutritional “ambrosia fungi” as their main source of food. The beetles are obligately dependent on their ambrosia fungi as they provide them a broad range of essential nutrients ensuring their survival in an extremely nutrient-poor environment. While xylem is rich in carbon (C) and hydrogen (H), various elements essential for fungal and beetle growth, such as nitrogen (N), phosphorus (P), sulfur (S), potassium (K), calcium (Ca), magnesium (Mg), and manganese (Mn) are extremely low in concentration. Currently it remains untested how both ambrosia beetles and their fungi meet their nutritional requirements in this habitat. Here, we aimed to determine for the first time if galleries of ambrosia beetles are generally enriched with elements that are rare in uncolonized xylem tissue and whether these nutrients are translocated to the galleries from the xylem by the fungal associates. To do so, we examined natural galleries of three ambrosia beetle species from three independently evolved farming lineages, Xyleborinus saxesenii (Scolytinae: Xyleborini), Trypodendron lineatum (Scolytinae: Xyloterini) and Elateroides dermestoides (Lymexylidae), that cultivate unrelated ambrosia fungi in the ascomycete orders Ophiostomatales, Microascales, and Saccharomycetales, respectively. Several elements, in particular Ca, N, P, K, Mg, Mn, and S, were present in high concentrations within the beetles’ galleries but available in only very low concentrations in the surrounding xylem. The concentration of elements was generally highest with X. saxesenii, followed by T. lineatum and E. dermestoides, which positively correlates with the degree of sociality and productivity of brood per gallery. We propose that the ambrosia fungal mutualists are translocating essential elements through their hyphae from the xylem to fruiting structures they form on gallery walls. Moreover, the extremely strong enrichment observed suggests recycling of these elements from the feces of the insects, where bacteria and yeasts might play a role. |
| first_indexed | 2024-12-17T19:08:55Z |
| format | Article |
| id | doaj.art-e1c5bd6473e34122a7db7443cf909090 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-17T19:08:55Z |
| publishDate | 2021-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-e1c5bd6473e34122a7db7443cf9090902022-12-21T21:35:56ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-04-011210.3389/fmicb.2021.664542664542Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched With Biologically Important ElementsMaximilian Lehenberger0Maximilian Lehenberger1Nina Foh2Axel Göttlein3Diana Six4Peter H. W. Biedermann5Peter H. W. Biedermann6Research Group Insect-Fungus Symbiosis, Department of Animal Ecology and Tropical Biology, University of Würzburg, Würzburg, GermanyChair of Forest Entomology and Protection, University of Freiburg, Freiburg im Breisgau, GermanyCenter for Medical Physics and Engineering, Max Schaldach Endowed Professorship for Biomedical Engineering, Friedrich-Alexander University Erlangen-Nürnberg (FAU), Erlangen, GermanyForest Nutrition and Water Resources, TUM School of Life Sciences Weihenstephan, Technical University of Munich, Freising, GermanyDepartment of Ecosystem and Conservation Sciences, W. A. Franke College of Forestry and Conservation, University of Montana, Missoula, MT, United StatesResearch Group Insect-Fungus Symbiosis, Department of Animal Ecology and Tropical Biology, University of Würzburg, Würzburg, GermanyChair of Forest Entomology and Protection, University of Freiburg, Freiburg im Breisgau, GermanyFungus-farming within galleries in the xylem of trees has evolved independently in at least twelve lineages of weevils (Curculionidae: Scolytinae, Platypodinae) and one lineage of ship-timber beetles (Lymexylidae). Jointly these are termed ambrosia beetles because they actively cultivate nutritional “ambrosia fungi” as their main source of food. The beetles are obligately dependent on their ambrosia fungi as they provide them a broad range of essential nutrients ensuring their survival in an extremely nutrient-poor environment. While xylem is rich in carbon (C) and hydrogen (H), various elements essential for fungal and beetle growth, such as nitrogen (N), phosphorus (P), sulfur (S), potassium (K), calcium (Ca), magnesium (Mg), and manganese (Mn) are extremely low in concentration. Currently it remains untested how both ambrosia beetles and their fungi meet their nutritional requirements in this habitat. Here, we aimed to determine for the first time if galleries of ambrosia beetles are generally enriched with elements that are rare in uncolonized xylem tissue and whether these nutrients are translocated to the galleries from the xylem by the fungal associates. To do so, we examined natural galleries of three ambrosia beetle species from three independently evolved farming lineages, Xyleborinus saxesenii (Scolytinae: Xyleborini), Trypodendron lineatum (Scolytinae: Xyloterini) and Elateroides dermestoides (Lymexylidae), that cultivate unrelated ambrosia fungi in the ascomycete orders Ophiostomatales, Microascales, and Saccharomycetales, respectively. Several elements, in particular Ca, N, P, K, Mg, Mn, and S, were present in high concentrations within the beetles’ galleries but available in only very low concentrations in the surrounding xylem. The concentration of elements was generally highest with X. saxesenii, followed by T. lineatum and E. dermestoides, which positively correlates with the degree of sociality and productivity of brood per gallery. We propose that the ambrosia fungal mutualists are translocating essential elements through their hyphae from the xylem to fruiting structures they form on gallery walls. Moreover, the extremely strong enrichment observed suggests recycling of these elements from the feces of the insects, where bacteria and yeasts might play a role.https://www.frontiersin.org/articles/10.3389/fmicb.2021.664542/fullambrosia beetleEcological stoichiometrymicrobiomenutrientsmacro- and micro-elementselement translocation |
| spellingShingle | Maximilian Lehenberger Maximilian Lehenberger Nina Foh Axel Göttlein Diana Six Peter H. W. Biedermann Peter H. W. Biedermann Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched With Biologically Important Elements Frontiers in Microbiology ambrosia beetle Ecological stoichiometry microbiome nutrients macro- and micro-elements element translocation |
| title | Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched With Biologically Important Elements |
| title_full | Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched With Biologically Important Elements |
| title_fullStr | Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched With Biologically Important Elements |
| title_full_unstemmed | Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched With Biologically Important Elements |
| title_short | Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched With Biologically Important Elements |
| title_sort | nutrient poor breeding substrates of ambrosia beetles are enriched with biologically important elements |
| topic | ambrosia beetle Ecological stoichiometry microbiome nutrients macro- and micro-elements element translocation |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.664542/full |
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