Mutualism is not restricted to tree‐killing bark beetles and fungi: the ecological stoichiometry of secondary bark beetles, fungi, and a scavenger

Abstract

1. All bark beetles are in symbiosis with fungi. Although obligate mutualisms with fungi are common with tree‐killing bark beetles (primaries), fungi associated with non‐tree‐killing bark beetles (secondaries) are usually dismissed as commensals. 2. Using an ecological stoichiometric approach, we show secondaries are also involved in nutrition‐based mutualisms, some of which appear obligate, and that differences in symbiont provisioning efficiency have a potent effect on beetle carbon (C): nitrogen (N): phosphorus (P) ratios. 3. Some secondary beetles have high P contents and require efficient P provisioning via fungi, while others have low P contents that may allow them to exploit less efficient fungi or a broader range of species with variable efficiencies. A co‐occurring scavenger that feeds on nutrient‐poor bark beetle frass (excrement/boring residues) exhibited the lowest phosphorus content yet recorded for an invertebrate. 4. Our results generally support the growth‐rate hypothesis that posits differences in C:P and N:P ratios in consumers are due to differential allocation of P to P‐rich RNA to support growth. However, while the beetle species that accumulated the most biomass was considerably enriched in P and that with the least biomass was P‐poor, one beetle species that was P‐rich was also small possibly due to limitation by an element other than P. 5. Our results indicate that fungi are important to a broader range of bark beetles than previously recognised. Additional research is needed to describe how these various symbioses influence forest ecosystems via differential effects of fungi on host beetle fitness.

Context Dependency in Bark Beetle-Fungus Mutualisms Revisited: Assessing Potential Shifts in Interaction Outcomes Against Varied Genetic, Ecological, and Evolutionary Backgrounds

“…While sapwood contains low amounts of N, P and NSC, its volume is massive compared to phloem. A fungal mycelium can potentially access the entirety of this resource while a beetle larva is confined to feeding in a small area of phloem ( Six and Elser, 2019 , 2020 ). Access to phloem is especially limited in beetle species that pack densely into trees due to mass attack behaviors.…”

“…Hylurgops porosus has low N and P demands and can develop in O. minus -colonized phloem. Even though this fungus is not highly efficient at concentrating these nutrients, its abilities are sufficient to support the beetle ( Six and Elser, 2020 ).…”

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

“…All herbivorous animals are confronted with a stoichiometric mismatch between the concentrations of elements required for growth and survival including nitrogen (N), phosphorus (P), potassium (K), calcium (Ca), magnesium (Mg), iron (Fe), zinc (Zn), manganese (Mn), copper (Cu) and sodium (Na), and those found in their plant diet, which is rich in only C, H, and O ( Sterner and Elser, 2002 ). For insects feeding within xylem this mismatch is extreme, as 99% of this tissue typically consists of C, H, and O ( Fengel and Wegener, 1989 ; Filipiak and Weiner, 2014 ) and elements such as N or P must be enriched by factors between 100 and 10,000 to support insect growth ( Six and Elser, 2020 ). Hence, they have only two options (or a combination of both); one is to develop very slowly and process massive amounts of plant material (see e.g., cerambycid or buprestid beetles) while the other is to supplement the diet with ectosymbiotic fungi that grow into the wood, and translocate and concentrate required elements for growth ( Buchner, 1928 ; Martin and Kukor, 1984 ; Filipiak and Weiner, 2014 ).…”

“…Basically, ES offers the opportunity to examine the availability and limitations of elements within natural systems and thus, is a useful tool to gain insights into tropic relations such as the ecology and function of insect-microbe mutualisms. Nevertheless, only very few studies applied ES to these systems ( Six and Elser, 2019 , 2020 ). Six and Elser (2019) examined for the very first time within a bark beetle species, how fungal mutualists associated with Dendroctonus brevicomis concentrate and translocate elements such as P and N from the sapwood and phloem to the bark, where the beetles live and feed.…”

Data_Sheet_1.xlsx

“…Apart from the questions raised above it would be interesting to investigate elemental accumulation from fungi growing in the galleries to the adult beetles and larvae (e.g., Six and Elser, 2020), which could give us insights into the specialization of ambrosia beetles to dead wood habitat. Furthermore, we need to determine how these elements may cycle within the gallery between beetles and their symbionts.…”