Nutrient-Poor Breeding Substrates of Ambrosia Beetles Are Enriched With Biologically Important Elements

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.

Lessons From Insect Fungiculture: From Microbial Ecology to Plastics Degradation

“…As sapwood constitute a nutrient-poor substrate, ambrosia fungal hyphae are thought to transport essential nutrients from the xylem, concentrating them in asexual fruiting structures forming the ambrosia layers. Calcium, nitrogen, phosphorus, potassium, magnesium, and sulfur are made available to ambrosia beetles by consuming such nutritious fruiting structures ( Fengel and Wegener, 2011 ; Filipiak and Weiner, 2014 ; Filipiak et al, 2016 ; Lehenberger et al, 2021b ). In addition, nutrients could be recycled from beetles’ feces through the crop and microbiota metabolic activity ( Batra, 1963 , 1967 ; Lehenberger et al, 2021b ).…”

“…Calcium, nitrogen, phosphorus, potassium, magnesium, and sulfur are made available to ambrosia beetles by consuming such nutritious fruiting structures ( Fengel and Wegener, 2011 ; Filipiak and Weiner, 2014 ; Filipiak et al, 2016 ; Lehenberger et al, 2021b ). In addition, nutrients could be recycled from beetles’ feces through the crop and microbiota metabolic activity ( Batra, 1963 , 1967 ; Lehenberger et al, 2021b ). Nitrogen derived from urea and uric acid in beetles feces could favor fungal growth, in turn providing essential amino acids, vitamins, and sterols to the beetles ( Batra, 1967 ; Norris and Baker, 1969 ; Kok et al, 1970 ; De Fine Licht and Biedermann, 2012 ; Lehenberger et al, 2021b ).…”

“…In addition, nutrients could be recycled from beetles’ feces through the crop and microbiota metabolic activity ( Batra, 1963 , 1967 ; Lehenberger et al, 2021b ). Nitrogen derived from urea and uric acid in beetles feces could favor fungal growth, in turn providing essential amino acids, vitamins, and sterols to the beetles ( Batra, 1967 ; Norris and Baker, 1969 ; Kok et al, 1970 ; De Fine Licht and Biedermann, 2012 ; Lehenberger et al, 2021b ). The metabolic profile of ambrosia fungi is mainly determined by their phylogenetic origin, likely optimized for the environmental niches they occupy.…”

The power of poop: Defecation behaviors and social hygiene in insects

“…Dark garden ants maintain fecal patches around the nest referred to as “kitchen middens,” which are not cleared out with other waste and are presumably treated by ants to limit microbial growth [ 14 ]. Additionally, ambrosia beetles, known for farming “ambrosia fungi,” may be provided essential elements by their obligate fungal symbiont through the recycling of fecal material ( Fig 1 ), with the highest concentrations of essential elements found to be positively correlated with the beetle’s level of sociality [ 15 ]. This correlation suggests that ambrosia beetles may benefit nutritionally from being more social and in closer association with a higher volume of feces.…”

First experimental evidence for active farming in ambrosia beetles and strong heredity of garden microbiomes

“…These yeast-like cultivars produce asexual fruiting structures only in the presence of the beetles and serve as their exclusive food source (25)(26)(27). Specifically, they provide their hosts with nutrients (i.e., vitamins, amino acids and sterols (28,29) and essential elements (N, P), which are translocated from the surrounding wood and are strongly concentrated within the fungal tissues the beetles feed on (30). Ambrosia fungus spores are vertically transmitted in the mycetangia (pouch-like structures) or guts of typically female beetles, when they disperse to found new nests and establish their own fungus gardens (31)(32)(33)(34).…”