Feedback systems from community interactions involving mutualisms are a rarely explored mechanism for generating complex population dynamics, including the cyclical behavior of many pest populations. We examined the effects of two linked mutualisms on the population dynamics of an outbreak bark beetle, Dendroctonus frontalis. D. frontalis are obligate mutualists with mycangial fungi. Tarsonemus mites, phoretic on D. frontalis, are strong mutualists with a bluestain fungus, Ophiostoma minus. Competitive interactions between associated fungi negatively affect D. frontalis larvae. These linked interactions potentially create an interaction system with the form of an endogenous negative feedback loop in which the abundance of beetles affects O. minus directly or indirectly through interactions with phoretic mites. Alternatively, the demographic effects of O. minus on beetles vary independently of beetle abundance. The variation in O. minus might be largely independent of mite abundance or partly driven by mite abundance.
Surveys of D. frontalis communities revealed that spatial patterns in abundance of mites and O. minus were a meaningful driver of spatial variation in beetle population dynamics; Tarsonemus, O. minus, and D. frontalis per capita reproduction covary in a manner consistent with strong indirect interactions from mites to O. minus to mycangial fungi to beetles. High mite and O. minus abundances were strongly correlated with beetle population decline and eventual extinction. Manipulation of beetle attack density and O. minus revealed strong negative effects of O. minus on beetle larvae, but the lack of an interaction between O. minus inoculation per beetle and beetle attack density falsified the hypothesis that horizontal transmission of O. minus generates negative demographic feedback. Instead, Tarsonemus and O. minus appeared to exert their effects on beetles independently of beetle density. The strong mutualism between Tarsonemus and O. minus likely contributes to the evolutionary maintenance of the antagonism between O. minus and D. frontalis. Co-occurrence of mutualisms embedded within a community may have stabilizing effects if both mutualisms limit each other. However, delays and/or non-linearities in the interaction systems may result in large population fluctuations, such as those displayed by D. frontalis.
Keywords: mutualism, population dynamics, keystone species, endogenous feedback, epidemic, phoretic mites