Emergent insects, pathogens and drought shape changing patterns in oak decline in North America and Europe

•The traditional sequence of events and factors involved in forest decline are changing.•Emergent insects, pathogens, and drought are involved in recent hardwood declines.•We examined the role of drought, forest history, and these agents in oak decline.•Climate extremes negatively affected tree carbon dynamics, resistance to biotic agents.•Relative to surviving oaks, those that died grew fast early during forest development.

Forest declines are well-studied phenomena. However, recent patterns suggest that the traditional sequence of events and factors involved in forest decline are changing. Several reports in recent decades involve emergent mortality agents, many of which are native insects and diseases. In addition, changing climate and weather patterns place increasing emphasis on root dynamics in forest decline, given the critical role of roots in susceptibility (loss of fine roots) and tolerance (deep-rooting) to drought. Contrasting successive extremes of wet and dry periods could negatively affect tree carbon (C) balance and water relations, which may provide an advantage to secondary agents such as root pathogens (e.g. Armillaria and Phytophthora spp.). We searched for patterns potentially implying mechanisms of mortality among several recent hardwood decline events (mostly in oak forests, Quercus spp.) linked to novel associations often involving drought – or hot drought, an apparent absence of defoliation, and a secondary bark- or wood-boring insect in a more aggressive tree-killing role than has been typically observed. To further explore one likely mechanism, we utilized a case study featuring an emergent mortality agent, the red oak borer, Enaphalodes rufulus (Haldeman) (Coleoptera: Cerambycidae), which, interacting with drought and forest history, resulted in an unprecedented oak mortality event (1999–2003, Ozark region, USA). Examination of long-term patterns of radial growth revealed that oaks surviving decline episodes often exhibited slow growth early during forest development, yet became superior competitors later on, and exhibited non-linear growth dynamics throughout their lives; trees that died often exhibited the opposite pattern, with rapid growth early in life and linear growth dynamics. We speculate that these different growth strategies could be related to patterns of resource allocation facilitated by root origins (sprout vs. seedling) and/or microsite conditions, and driven or influenced by repeated drought. Carbon balance dysfunction, a long-term affliction of oaks that eventually manifests itself in an episode of decline, may be the underlying mechanism of oak mortality during decline. It is likely caused by changes in C supply and demand during drought and/or defoliation that compromise oaks by depleting C reserves, or somehow inhibiting translocation of stored C to repair damaged tissues and resist secondary biotic agents. Ultimately, successive drought and persistent activity by these insects and pathogens kill affected oaks. Parallels among different hardwood ecosystems exist, and can be used to help predict future scenarios and guide new avenues of study.

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