Epidemiology and Physiological Impact of Aerial Phytophthora pluvialis in New Zealand and Oregon Forest Systems
Forest health is threatened by invasive plant-infecting fungi and fungal-like organisms, whose frequency has increased with international trade in recent decades. While planted forests are particularly vulnerable to invasive pathogens, the area under production is increasing due to the growing world population and the subsequent growing demand of fibre. Phytophthora species are a remarkable group of pathogens in agricultural and forest systems. Over the past few decades, numerous members of this genus have been reported to affect conifer plantations as foliar pathogens. Phytophthora pluvialis is the causal agent of red needle cast disease (RNC) affecting Pinus radiata plantations in New Zealand (NZ) since 2008. The pathogen was described as a new species following its recovery from baited stream and soils from mixed tanoak and Douglas-fir (Pseudotsuga menziesii) forests in southwestern Oregon (US). More recently, P. pluvialis has been associated with early defoliation in Douglas-fir in both countries. This thesis had two main objectives: (1) to gain knowledge on the epidemiology of P. pluvialis in the two hosts in NZ and Oregon forests systems, and (2) to analyse the physiological impact of P. pluvialis infection on the host. Detached-needle assays and on-plant inoculations were performed on radiata pine to analyse the key drivers of the RNC disease. The data was fitted into an epidemiological model extended to account for the dynamics of the pathogen on the infected needles. Primary infection presented a peak 4 days after inoculation, from which polycyclic infections developed reaching a peak 22 days after inoculation. Susceptible and resistant genotypes differed in the pathogen death rate (2.5 times lower in susceptible genotypes), and higher presence of external proliferation of mycelium and sporangia (90% vs 25% of the infected needles). Real-time PCR (qPCR) effectively detected P. pluvialis earlier after inoculation, but it was less efficient at later stages of the epidemic, than isolations. Isolations were not influenced by the presence of lesions, while 19% of lesioned needle maximized qPCR detection. In Douglas-fir, detached-needle and -twig assays showed the co-infection of needles by both P. pluvialis and the ascomycete fungus Nothophaeocryptopus gaeumannii, which is the cause of the Swiss needle cast disease globally. The coexistence of both pathogens was confirmed in NZ and the US Pacific Northwest (PNW) at different spatial scales ranging from the needles to the region. Both pathogens were more abundant in the host’s exotic environment, NZ, in contrast to its endemic range of the PNW. Their relative abundance was negatively correlated in the PNW, where both pathogens are presumed to have coexisted for longer. Higher winter relative humidity values led to larger P. pluvialis abundance in Douglas-fir. The physiological impact of needle loss associated with RNC was studied in an artificial inoculation experiment simulating the defoliation pattern of the disease. Two RNC-susceptible genotypes were treated. Growth and carbon (C) allocation in the genotype with initial higher specific leaf area were unaffected by defoliation. In contrast, the other genotype suffered C shortage. Diameter of radiata pine at 3 cm up from the graft union was 23% and 32% lower in defoliated plants one and two growing seasons after defoliation, respectively. Height and total aboveground biomass reductions of 36% and 55%, respectively, were only noted after the second growing season following defoliation. A decrease in sugar storage in roots during canopy development, followed by a recovery in root sugar reserves were also observed after the second growing season following defoliation. Trees affected by RNC seem to recover after canopy development, but the reduction in growth and transient reductions in C reserves may make them more vulnerable to other biotic or abiotic stressors. RNC impact on host’s productivity and resilience should be analysed through an integrative approach. Compartmental models offer a great opportunity to integrate within a common framework several disciplines needed to implement smarter disease management strategies: plant pathology, ecophysiology, chemistry and forest economy.