Roots Mediate the Effects of Snowpack Decline on Soil Bacteria, Fungi, and Nitrogen Cycling in a Northern Hardwood Forest.

Rising winter air temperature will reduce snow depth and duration over the next century in northern hardwood forests. Reductions in snow depth may affect soil bacteria and fungi directly, but also affect soil microbes indirectly through effects of snowpack loss on plant roots. We incubated root exclusion and root ingrowth cores across a winter climate-elevation gradient in a northern hardwood forest for 29 months to identify direct (i.e., winter snow-mediated) and indirect (i.e., root-mediated) effects of winter snowpack decline on soil bacterial and fungal communities, as well as on potential nitrification and net N mineralization rates. Both winter snowpack decline and root exclusion increased bacterial richness and phylogenetic diversity. Variation in bacterial community composition was best explained by differences in winter snow depth or soil frost across elevation. Root ingrowth had a positive effect on the relative abundance of several bacterial taxonomic orders (e.g., Acidobacterales and Actinomycetales). Nominally saprotrophic (e.g., Saccharomycetales and Mucorales) or mycorrhizal (e.g., Helotiales, Russalales, Thelephorales) fungal taxonomic orders were also affected by both root ingrowth and snow depth variation. However, when grouped together, the relative abundance of saprotrophic fungi, arbuscular mycorrhizal fungi, and ectomycorrhizal fungi were not affected by root ingrowth or snow depth, suggesting that traits in addition to trophic mode will mediate fungal community responses to snowpack decline in northern hardwood forests. Potential soil nitrification rates were positively related to ammonia-oxidizing bacteria and archaea abundance (e.g., Nitrospirales, Nitrosomondales, Nitrosphaerales). Rates of N mineralization were positively and negatively correlated with ectomycorrhizal and saprotrophic fungi, respectively, and these relationships were mediated by root exclusion. The results from this study suggest that a declining winter snowpack and its effect on plant roots each have direct effects on the diversity and abundance of soil bacteria and fungal communities that interact to determine rates of soil N cycling in northern hardwood forests.

Reduced snow cover alters root-microbe interactions and decreases nitrification rates in a northern hardwood forest.

Snow cover is projected to decline during the next century in many ecosystems that currently experience a seasonal snowpack. Because snow insulates soils from frigid winter air temperatures, soils are expected to become colder and experience more winter soil freeze-thaw cycles as snow cover continues to decline. Tree roots are adversely affected by snowpack reduction, but whether loss of snow will affect root-microbe interactions remains largely unknown. The objective of this study was to distinguish and attribute direct (e.g., winter snow- and/or soil frost-mediated) vs. indirect (e.g., root-mediated) effects of winter climate change on microbial biomass, the potential activity of microbial exoenzymes, and net N mineralization and nitrification rates. Soil cores were incubated in situ in nylon mesh that either allowed roots to grow into the soil core (2 mm pore size) or excluded root ingrowth (50 µm pore size) for up to 29 months along a natural winter climate gradient at Hubbard Brook Experimental Forest, NH (USA). Microbial biomass did not differ among ingrowth or exclusion cores. Across sampling dates, the potential activities of cellobiohydrolase, phenol oxidase, and peroxidase, and net N mineralization rates were more strongly related to soil volumetric water content (P < 0.05; R2  = 0.25-0.46) than to root biomass, snow or soil frost, or winter soil temperature (R2  < 0.10). Root ingrowth was positively related to soil frost (P < 0.01; R2  = 0.28), suggesting that trees compensate for overwinter root mortality caused by soil freezing by re-allocating resources towards root production. At the sites with the deepest snow cover, root ingrowth reduced nitrification rates by 30% (P < 0.01), showing that tree roots exert significant influence over nitrification, which declines with reduced snow cover. If soil freezing intensifies over time, then greater compensatory root growth may reduce nitrification rates directly via plant-microbe N competition and indirectly through a negative feedback on soil moisture, resulting in lower N availability to trees in northern hardwood forests.

Winter climate change affects growing-season soil microbial biomass and activity in northern hardwood forests.

Understanding the responses of terrestrial ecosystems to global change remains a major challenge of ecological research. We exploited a natural elevation gradient in a northern hardwood forest to determine how reductions in snow accumulation, expected with climate change, directly affect dynamics of soil winter frost, and indirectly soil microbial biomass and activity during the growing season. Soils from lower elevation plots, which accumulated less snow and experienced more soil temperature variability during the winter (and likely more freeze/thaw events), had less extractable inorganic nitrogen (N), lower rates of microbial N production via potential net N mineralization and nitrification, and higher potential microbial respiration during the growing season. Potential nitrate production rates during the growing season were particularly sensitive to changes in winter snow pack accumulation and winter soil temperature variability, especially in spring. Effects of elevation and winter conditions on N transformation rates differed from those on potential microbial respiration, suggesting that N-related processes might respond differently to winter climate change in northern hardwood forests than C-related processes.

The fate of nitrogen in gypsy moth frass deposited to an oak forest floor.

Forest defoliation by insects can lead to severe disruptions of the nitrogen (N) cycle resulting in elevated NO3- levels in stream water. To trace the movement of insect-mobilized N in a forest soil, 15N-labeled gypsy moth frass or 15N-labeled oak leaf litter was added to trenched plots in an oak forest over 29 months. Nitrogen movement from the frass or litter was measured in the available, mineralizable, microbial and total soil pools. Uptake of 15N by oak seedlings and inorganic N leaching losses were also measured. No significant differences were found between the frass or leaf treatments for total N in any of the pools. Significant differences were found among the treatments in the distribution of the 15N tracer. Forty percent of the 15N added as frass became incorporated in the soils, with less than 1% found in oak seedlings. Almost 80% of 15N added as leaves remained in the undecomposed leaf material after 2 years. Less than 0.001% of the added 15N was leached in both treatments. Our data indicate that N in frass is mobilized more quickly than N in leaf litter. However, this frass N may be largely unavailable to plants and microorganisms as little of it was found in the extractable, microbial, or readily mineralizable pools.

Caterpillar guts and ammonia volatilization: retention of nitrogen by gypsy moth larvae consuming oak foliage.

The gypsy moth (Lymantria dispar L.), a major defoliator of hardwood forests in the eastern U.S., has a highly alkaline midgut pH. We hypothesized that the high pH would cause high rates of ammonia (NH3) volatilization as larvae consumed foliage, leading to potentially large losses of N from the ecosystem to the atmosphere during gypsy moth outbreaks. We measured NH3 emission during the consumption of oak foliage by larvae in the laboratory. Surprisingly, we found very low amounts of NH3 release of about 0.1% of the N consumed in foliage. We speculate that digestive mechanisms may limit NH3 production in the midgut, and that the acidic environment of the hindgut traps most of the small amount of NH3 that is produced, effectively preventing a potentially very large N loss from both larvae and ecosystem. The estimated rate of NH3 emission from a defoliated forest is small compared to other inputs and outputs of N from the ecosystem, but could potentially enhance the neutralization of atmospheric acidity during the defoliation period.