Invasive forest pathogens affect the characteristics, microbial colonisation, and decomposition of leaf litter in streams

Abstract

Invasive tree pathogens threaten forests worldwide, but their effects on streams are poorly understood. Nevertheless, tree infections that lead to changes in the characteristics of litter inputs to streams may affect stream communities and ecosystem processes. We studied cross‐ecosystem effects derived from Phytophthora cinnamomi, Phytophthora ×alni, and Ophiostoma novo‐ulmi infection on Castanea sativa (chestnut), Alnus lusitanica (alder), and Ulmus minor (elm) trees, respectively, by assessing physical and chemical characteristics of senescent leaves from healthy, symptomatic, and highly symptomatic individuals. Leaf litter from the three health statuses per tree species was then incubated in laboratory microcosms and the effects of tree infection on microbial decomposers and leaf litter decomposition were assessed. Tree infection significantly affected leaf litter characteristics, microbial decomposers and leaf litter decomposition, and the health status of trees conditioned these effects differently depending on the tree species. In C. sativa, leaf litter of highly symptomatic trees had higher toughness, higher polyphenolic concentration and slower decomposition than leaf litter of symptomatic and healthy trees. In A. lusitanica, leaf litter of highly symptomatic trees had higher phosphorus concentration, lower carbon:phosphorus ratio and faster decomposition than leaf litter of symptomatic and healthy trees. Finally, in U. minor, leaf litter of highly symptomatic trees had higher nitrogen concentration and lower carbon:nitrogen ratio than leaf litter of healthy trees, and faster decomposition than leaf litter of symptomatic and healthy trees. Effects of changes in litter characteristics on litter decomposition were mediated by changes in microbial decomposer colonisation and activity. The composition of the aquatic hyphomycetes communities associated with C. sativa and U. minor litter varied depending on the tree health status. Most striking was the two‐fold higher aquatic hyphomycetes species richness in litter of U. minor trees infected with O. novo‐ulmi than in litter of healthy U. minor trees. Tree infection alters the nutritional quality of leaf litter, potentially affecting the functioning of aquatic ecosystems strongly dependent on riparian litter inputs.

Climate‐induced plasticity in leaf traits of riparian plants

“…Nonetheless, apparent subtle changes in litter traits might result in major effects in consumer fitness (Pérez et al, 2021). Furthermore, this projected minor decrease in leaf quality adds to the decline of populations of this key species through Europe due to a disease caused by the pathogen Phytophthora alni (Bjelke et al, 2016), which also has been recently reported to alter the nutritional quality of leaf litter (Ferreira et al, 2021). Both factors are likely to trigger significant alterations to the functioning of forested streams (Alonso et al, 2021).…”

Dieback and Replacement of Riparian Trees May Impact Stream Ecosystem Functioning

“…At the southern limit of P . × alni distribution, occurring in Jerte river (Plasencia, Spain) [ 24 ] and Ceira river (Arouce, Portugal) [ 25 ], disease severity is lower than in the north. Tree infection is produced by zoospores in the roots or in the trunk during floods, leading to root rot, collar rot, small-size, sparse and often chlorotic foliage, crown dieback, and tree mortality.…”

“…Mortality rates reach almost 100%, with young trees usually dying in few months and old trees dying in years while losing vitality progressively [ 18 , 19 ]. Leaf litter of Alnus lusitanica Vít, Douda and Mandák infected trees has higher nutrient concentration than that from healthy trees due to reduced nutrient resorption before senescence, leading to fast decomposition of leaf litter [ 24 ].…”

“…To explore differences among native ash, native poplar, healthy and infected native alder, and invasive black locust, and facilitate the understanding of interactions in leaf mixtures, including diversity effects on decomposition and fungal biomass, monocultures of all leaf litter types were also assessed. Based on the main traits of different leaf litter types, we hypothesized the following: Scenario 2, with infected alder, would show higher leaf litter decomposition rate, fungal biomass, and fungal sporulation rate than scenario 1, with healthy alder, since leaf litter of infected alder is richer in nutrients and more labile [ 24 ], thus possibly enhancing decomposition and fungal activity in mixtures [ 12 ]. Scenario 3, with black locust, would show lower leaf litter decomposition rate, fungal biomass, and fungal sporulation rate than scenarios 1 and 2 (with healthy and infected alder, respectively), because of the higher lignin and polyphenol concentration in black locust leaf litter, which potentially slows down decomposition and fungal activity in mixtures [ 12 ], despite both black locust and alder having high concentration of nutrients [ 33 , 34 ].…”

“… Scenario 3, with black locust, would show lower leaf litter decomposition rate, fungal biomass, and fungal sporulation rate than scenarios 1 and 2 (with healthy and infected alder, respectively), because of the higher lignin and polyphenol concentration in black locust leaf litter, which potentially slows down decomposition and fungal activity in mixtures [ 12 ], despite both black locust and alder having high concentration of nutrients [ 33 , 34 ]. Fungal assemblages would be altered in scenarios 2 and 3 compared with scenario 1, due to strong substrate preferences of fungal microorganisms [ 11 ], the change being higher under scenario 3 than under scenario 2 because fungi would be more affected by species composition change [ 12 ] than by alder infection [ 24 ]. …”