Urbanization and edge effects interact to drive mutualism breakdown and the rise of unstable pathogenic communities in forest soil.

Temperate forests are threatened by urbanization and fragmentation, with over 20% (118,300 km2) of U.S. forest land projected to be subsumed by urban land development. We leveraged a unique, well-characterized urban-to-rural and forest edge-to-interior gradient to identify the combined impact of these two land use changes-urbanization and forest edge creation-on the soil microbial community in native remnant forests. We found evidence of mutualism breakdown between trees and their fungal root mutualists [ectomycorrhizal (ECM) fungi] with urbanization, where ECM fungi colonized fewer tree roots and had less connectivity in soil microbiome networks in urban forests compared to rural forests. However, urbanization did not reduce the relative abundance of ECM fungi in forest soils; instead, forest edges alone led to strong reductions in ECM fungal abundance. At forest edges, ECM fungi were replaced by plant and animal pathogens, as well as copiotrophic, xenobiotic-degrading, and nitrogen-cycling bacteria, including nitrifiers and denitrifiers. Urbanization and forest edges interacted to generate new "suites" of microbes, with urban interior forests harboring highly homogenized microbiomes, while edge forest microbiomes were more heterogeneous and less stable, showing increased vulnerability to low soil moisture. When scaled to the regional level, we found that forest soils are projected to harbor high abundances of fungal pathogens and denitrifying bacteria, even in rural areas, due to the widespread existence of forest edges. Our results highlight the potential for soil microbiome dysfunction-including increased greenhouse gas production-in temperate forest regions that are subsumed by urban expansion, both now and in the future.

Elevated growth and biomass along temperate forest edges.

Fragmentation transforms the environment along forest edges. The prevailing narrative, driven by research in tropical systems, suggests that edge environments increase tree mortality and structural degradation resulting in net decreases in ecosystem productivity. We show that, in contrast to tropical systems, temperate forest edges exhibit increased forest growth and biomass with no change in total mortality relative to the forest interior. We analyze >48,000 forest inventory plots across the north-eastern US using a quasi-experimental matching design. At forest edges adjacent to anthropogenic land covers, we report increases of 36.3% and 24.1% in forest growth and biomass, respectively. Inclusion of edge impacts increases estimates of forest productivity by up to 23% in agriculture-dominated areas, 15% in the metropolitan coast, and +2% in the least-fragmented regions. We also quantify forest fragmentation globally, at 30-m resolution, showing that temperate forests contain 52% more edge forest area than tropical forests. Our analyses upend the conventional wisdom of forest edges as less productive than intact forest and call for a reassessment of the conservation value of forest fragments.

Current and future biomass carbon uptake in Boston's urban forest.

Ecosystem services provided by urban forests are increasingly included in municipal-level responses to climate change. However, the ecosystem functions that generate these services, such as biomass carbon (C) uptake, can differ substantially from nearby rural forest. In particular, the scaled effect of canopy spatial configuration on tree growth in cities is uncertain, as is the scope for medium-term policy intervention. This study integrates high spatial resolution data on tree canopy and biomass in the city of Boston, Massachusetts, with local measurements of tree growth rates to estimate the magnitude and distribution of annual biomass C uptake. We further project C uptake, biomass, and canopy cover change to 2040 under alternative policy scenarios affecting the planting and preservation of urban trees. Our analysis shows that 85% of tree canopy area was within 10 m of an edge, indicating essentially open growing conditions. Using growth models accounting for canopy edge effects and growth context, Boston's current biomass C uptake may be approximately double (median 10.9 GgC yr-1, 0.5 MgC ha-1 yr-1) the estimates based on rural forest growth, much of it occurring in high-density residential areas. Total annual C uptake to long-term biomass storage was equivalent to <1% of estimated annual fossil CO2 emissions for the city. In built-up areas, reducing mortality in larger trees resulted in the highest predicted increase in canopy cover (+25%) and biomass C stocks (236 GgC) by 2040, while planting trees in available road margins resulted in the greatest predicted annual C uptake (7.1 GgC yr-1). This study highlights the importance of accounting for the altered ecosystem structure and function in urban areas in evaluating ecosystem services. Effective municipal climate responses should consider the substantial fraction of total services performed by trees in developed areas, which may produce strong but localized atmospheric C sinks.