Abstract
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.
Highlights
In 1836, the monk Josef Schmidberger noticed a whitish layer in tunnel systems of some scolytine beetles within the sap- and heartwood of his apple trees (Schmidberger, 1836)
The semi-quantitative scanning electron microscope (SEM)-energy dispersive X-ray detector (EDX) analysis revealed that all examined galleries [3 × X. saxesenii, (Figures 1, 2 and Supplementary Figures 1, 2); 2 × T. lineatum, (Figures 3, 4 and Supplementary Figure 3); 1 × E. dermestoides, (Figure 5)] were enriched with N, Mg, P, S, K, and Ca
Mg could not be identified within one of the three galleries of X. saxesenii using SEM-EDX, but the presences of this element within this specific gallery was proven by the EDX-Mapping function
Summary
In 1836, the monk Josef Schmidberger noticed a whitish layer in tunnel systems of some scolytine beetles within the sap- and heartwood (i.e., xylem) of his apple trees (Schmidberger, 1836). Common to all of them is their species-specific, obligate nutritional mutualism with filamentous fungi, which they transmit vertically in mycetangia (extracuticular sporecarrying organs; see Francke-Grosmann, 1956) and more or less actively farm in often social family groups (but Lymexylidae are solitary; Francke-Grosmann, 1967; Beaver, 1989; Kirkendall et al, 2015; Hulcr and Stelinski, 2017; Biedermann and Vega, 2020) Their mutualistic fungi are from at least five ascomycete (Ophiostomataceae, Ceratocystidaceae, Nectriaceae, Bionectriaceae, Saccharomycetaceae) and two basidiomycete (Peniophoraceae, Meruliaceae) (Hulcr and Stelinski, 2017; Biedermann and Vega, 2020) families. They strongly depend on the beetle for dispersal, are not capable of surviving outside the mutualism, produce nutrient-rich fruiting structures within the beetles’ galleries, and are the sole or at least major food source for the beetles (Neger, 1908a,b; Batra, 1963, 1966, 1967, 1973, 1985; Francke-Grosmann, 1966, 1967; Batra, 1967)
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