Disease in regenerating pine forests linked to temperature and pathogen spillover from the canopy

Abstract

1. Previous investigations of the role of pathogens as drivers of community dynamics in forests have mostly focused on interspecific interactions between canopy trees and seedlings via soil feedbacks. However, feedbacks can also occur directly between canopy trees and seedlings when spores of foliar and stem pathogens fall onto seedlings regenerating underneath the canopy.2. We studied pathogen spillover between canopy trees and conspecific and heterospecific regeneration in the Pinus nigra-Diplodia sapinea pathosystem. We sampled 70 pine stands distributed across a temperature gradient of 9.5-13.7°C(mean annual temperature). In each stand, we linked spore load and spore survival in the canopy with pathogen biomass and disease severity in regenerating seedlings. The density of regenerating seedlings and the health status of conspecific and heterospecific seedlings were also measured. The strength of canopy-understorey interactions was correlated with both climatic and stand variables.3. The most severe symptoms of disease in regenerating seedlings were found in the warmest stands. Structural equation models suggested that disease severity in seedlings was mediated by an increased spore spillover from the canopy.Temperature also increased the pathogen survival rate within seedlings, further contributing to disease severity. Interestingly, disease severity in the canopy did not correlate with spore load in the canopy, suggesting that adult trees were spilling pathogens onto the understorey regardless of their health status.Pathogen spillover increased in more open stands. Greater disease severity in seedlings correlated with stands with a higher density of oak seedlings. 4. Synthesis. These results suggest an understudied mechanism of the Janzen-Connell theory, according to which, canopy-understorey negative feedbacks could be driven by canopy pathogens. Our data also suggest that temperature shapes canopy-understorey interactions, which implies that under a warming climate scenario, an acceleration of conspecific negative feedbacks could be expected, with implications for forest regeneration dynamics.

Effects of tree species diversity and conspecific seedling density on insect herbivory and pathogen infection on big‐leaf mahogany seedlings

“…This result is consistent with previous work showing reductions in attack rates by specialist plant enemies, including both insects (Castagneyrol et al 2013, Abdala-Roberts et al 2015, reviewed by Moreira et al 2016) and fungal plant pathogens (Mitchell et al 2002, Hantsch et al 2014, Rutten et al 2021, with increasing plant diversity. Further, it provides evidence for poorly studied understory-canopy negative feedbacks among conspecifics via pathogens as adult trees were the main source of seedling infection in this study (Caballol et al 2022). It is important to note, however, that our experimental design testing for tree diversity effects does not separate mahogany tree density (number of individual trees per plot) versus frequency (proportion or abundance of mahogany trees relative to heterospecifics per plot) effects, two important sources of variation which could have contributed to reductions in seedling pathogen infection rates in polyculture.…”

“…Studies that manipulate plant density across different levels of tree diversity or composition are needed to better understand variation in enemy responses to host plant abundance as a function of the tree community context and its underlying mechanisms. For example, adult density of a focal species can vary as a function of tree diversity and has been shown to be an important driver of enemy attack on conspecific seedlings due to canopy-to-understory enemy spill over (Caballol et al 2022). Such effects would presumably operate via one or more of the mechanisms mentioned previously, including resource concentration or associational effects.…”

Climate acts as an environmental filter to plant pathogens

“…The ability to cope with dry conditions seems to be key to colonizing southern latitudes whereas the ability to survive under cold conditions seems to be key for colonizing northern latitudes. Our analyses highlight the role played by climate in the distribution of pathogens besides their parasitic lifestyle and may explain why native and exotic pathogens often do not completely cover the range of their hosts [ 49 ].…”

First report of Diplodia sapinea causing Diplodia tip blight on Juniperus communis subsp. communis in Finland

“…2022 possibly related to the high load of spores from the canopy (Caballol et al. , 2022). Diplodia sapinea is a new, broad‐host opportunistic pathogen in Finland and the disease Diplodia tip blight can be expected to increase in alternative hosts, especially in areas that are vulnerable to abiotic changes (for example, drought).…”

“…Diplodia sapinea can be endophytic and may turn pathogenic in droughtstressed trees (Blumenstein et al, 2022). Accumulating data suggest that D. sapinea is an opportunistic pathogen which also infects alternative host species Blumenstein et al 2022 possibly related to the high load of spores from the canopy (Caballol et al, 2022). Diplodia sapinea is a new, broad-host opportunistic pathogen in Finland and the disease Diplodia tip blight can be expected to increase in alternative hosts, especially in areas that are vulnerable to abiotic changes (for example, drought).…”