Strong Interactive Effects of Warming and Insect Herbivory on Soil Carbon and Nitrogen Dynamics at Subarctic Tree Line

Warming will likely stimulate Arctic primary production, but also soil C and N mineralization, and it remains uncertain whether the Arctic will become a sink or a source for CO2. Increasing insect herbivory may also dampen the positive response of plant production and soil C input to warming. We conducted an open-air warming experiment with Subarctic field layer vegetation in North Finland to explore the effects of warming (+3°C) and reduced insect herbivory (67% reduction in leaf damage using an insecticide) on soil C and N dynamics. We found that plant root growth, soil C and N concentrations, microbial biomass C, microbial activity, and soil NH4+ availability were increased by both warming and reduced herbivory when applied alone, but not when combined. Soil NO3– availability increased by warming only and in-situ soil respiration by reduced herbivory only. Our results suggest that increasing C input from vegetation under climate warming increases soil C concentration, but also stimulates soil C turnover. On the other hand, it appears that insect herbivores can significantly reduce plant growth. If their abundance increases with warming as predicted, they may curtail the positive effect of warming on soil C concentration. Moreover, our results suggest that temperature and herbivory effects on root growth and soil variables interact strongly, which probably arises from a combination of N demand increasing under lower herbivory and soil mineral N supply increasing under higher temperature. This may further complicate the effects of rising temperatures on Subarctic soil C dynamics.</p

Strong Interactive Effects of Warming and Insect Herbivory on Soil Carbon and Nitrogen Dynamics at Subarctic Tree Line

Warming will likely stimulate Arctic primary production, but also soil C and N mineralization, and it remains uncertain whether the Arctic will become a sink or a source for CO2. Increasing insect herbivory may also dampen the positive response of plant production and soil C input to warming. We conducted an open-air warming experiment with Subarctic field layer vegetation in North Finland to explore the effects of warming (+3 degrees C) and reduced insect herbivory (67% reduction in leaf damage using an insecticide) on soil C and N dynamics. We found that plant root growth, soil C and N concentrations, microbial biomass C, microbial activity, and soil NH4+ availability were increased by both warming and reduced herbivory when applied alone, but not when combined. Soil NO3- availability increased by warming only and in-situ soil respiration by reduced herbivory only. Our results suggest that increasing C input from vegetation under climate warming increases soil C concentration, but also stimulates soil C turnover. On the other hand, it appears that insect herbivores can significantly reduce plant growth. If their abundance increases with warming as predicted, they may curtail the positive effect of warming on soil C concentration. Moreover, our results suggest that temperature and herbivory effects on root growth and soil variables interact strongly, which probably arises from a combination of N demand increasing under lower herbivory and soil mineral N supply increasing under higher temperature. This may further complicate the effects of rising temperatures on Subarctic soil C dynamics.Peer reviewe

Higher vascular plant abundance associated with decreased ecosystem respiration after 20 years of warming in the forest-tundra -ecotone

&lt;p&gt;&lt;span&gt;The ongoing climate warming is promoting shrub abundance in high latitudes, but the effect of this phenomenon on ecosystem functioning is expected to depend on whether deciduous or evergreen species increase in response to warming. &lt;/span&gt;&lt;/p&gt; &lt;p&gt;&lt;span&gt;To explore effects of long-term warming on shrubs and further on ecosystem functioning, we analyzed vegetation and ecosystem CO&lt;sub&gt;2&lt;/sub&gt; exchange after 20 years of warming in the forest-tundra ecotone in sub-arctic Sweden. A previous study conducted nine years earlier had found increased evergreen &lt;em&gt;Empetrum&lt;/em&gt; &lt;em&gt;nigrum&lt;/em&gt; ssp. &lt;em&gt;hermaphroditum&lt;/em&gt; in the forest and increased deciduous &lt;em&gt;Betula&lt;/em&gt; &lt;em&gt;nana&lt;/em&gt; in the tundra. &lt;/span&gt;&lt;/p&gt; &lt;p&gt;&lt;span&gt;Following current understanding, we expected a continued increase in shrub abundance that would be stronger in tundra than in forest. We expected warming to increase ecosystem respiration (&lt;/span&gt;&lt;span&gt;R&lt;sub&gt;e&lt;/sub&gt;&lt;/span&gt;&lt;span&gt;) and gross primary productivity (GPP), with a greater increase in &lt;/span&gt;&lt;span&gt;R&lt;sub&gt;e &lt;/sub&gt;in tundra due to increased deciduous shrub abundance, leading to a less negative net ecosystem exchange (NEE) and reduced ecosystem C sink strength. &lt;/span&gt;&lt;/p&gt; &lt;p&gt;&lt;span&gt;As predicted, vascular plant abundances were higher in the warmed plots with a stronger response in tundra than in forest. &lt;/span&gt;&lt;span&gt;However, whereas &lt;em&gt;B. nana&lt;/em&gt; had increased in abundance since the last survey, &lt;em&gt;E. hermaphroditum &lt;/em&gt;abundance had declined due to several moth and rodent outbreaks during the past decade. &lt;/span&gt;&lt;span&gt;I&lt;/span&gt;&lt;span&gt;n contrast to predictions, &lt;/span&gt;&lt;span&gt;R&lt;sub&gt;e &lt;/sub&gt;was significantly lower in the warmed plots irrespective of habitat, and GPP increased marginally only in the forest. The lower R&lt;sub&gt;e&lt;/sub&gt; and a higher GPP under warming in the forest together led to increased net C sink. &lt;/span&gt;&lt;span&gt;R&lt;sub&gt;e &lt;/sub&gt;was negatively associated with the total vascular plant abundance.&lt;/span&gt;&lt;/p&gt; &lt;p&gt;&lt;span&gt;Our results highlight the importance of disturbance regimes for vegetation responses to warming. &lt;/span&gt;&lt;span&gt;Climate warming may promote species with &lt;/span&gt;&lt;span&gt;both a high capacity to grow under warmer conditions and a resilience towards herbivore outbreaks. Negative correlation between R&lt;sub&gt;e&lt;/sub&gt; and total vascular plant abundance further indicates that t&lt;/span&gt;&lt;span&gt;he &lt;/span&gt;&lt;span&gt;indirect impacts of increased plants on soil microclimate may become increasingly important for ecosystem CO&lt;sub&gt;2&lt;/sub&gt; exchange &lt;/span&gt;&lt;span&gt;in the long &lt;/span&gt;&lt;span&gt;run&lt;/span&gt;&lt;span&gt;, &lt;/span&gt;&lt;span&gt;which adds to the different mechanisms that link warming and CO&lt;sub&gt;2&lt;/sub&gt; fluxes in northern ecosystems.&lt;/span&gt;&lt;/p&gt;&lt;p&gt;Funding provided by: Academy of Finland&lt;br&gt;Crossref Funder Registry ID: https://ror.org/05k73zm37&lt;br&gt;Award Number: 310776&lt;/p&gt;&lt;p&gt;Funding provided by: Finnish Cultural Foundation&lt;br&gt;Crossref Funder Registry ID: https://ror.org/027xav248&lt;br&gt;Award Number: 40221879&lt;/p&gt;&lt;p class="MsoNormal"&gt;&lt;em&gt;&lt;span&gt;Vegetation analyses&lt;/span&gt;&lt;/em&gt;&lt;/p&gt; &lt;p class="MsoNormal"&gt;&lt;span&gt;The plant community composition was earlier recorded in 1999 and 2009 in five control plots and five OTCs in both habitats (Kaarlejärvi et al. 2012). We used the same plots during the present investigation and analyzed the composition of vegetation in July 2018 with the point intercept method: in OTCs, a total of 87 pins was systematically distributed among three diagonals of the hexagons, 29 pins per diagonal. For each pin, the total number of hits as well as the height of the highest hit were recorded for each plant. Only one hit for each species was counted at the ground layer for each pin. The same method was applied to control plots. Later the total number of hits was normalized to hits per 100 pins. Data from one forest plot was discarded because of poor plot condition.&lt;/span&gt;&lt;/p&gt; &lt;p class="MsoNormal"&gt;&lt;em&gt;&lt;span&gt;Ecosystem carbon flux analyses&lt;/span&gt;&lt;/em&gt;&lt;/p&gt; &lt;p class="MsoNormal"&gt;&lt;span&gt;For the ecosystem carbon flux analyses, we included a few additional plots to have seven plots per treatment in the forest and eight plots per treatment in the tundra. The fluxes were analyzed at two-week intervals throughout the growing season 2018 (from 5&lt;sup&gt;th&lt;/sup&gt; of June to 19&lt;sup&gt;th&lt;/sup&gt; of August) using a closed system composed of a custom-built acrylic chamber (diameter 146 cm, height 60 cm) coupled to a Vaisala Carbon Dioxide Probe GMP343, Vaisala Humidity and Temperature Probe HMP75 and Vaisala Measurement Indicator MI70. Measurements included four consecutive measures of gradually changing light intensity: ambient light, 35% and 60% shading, and darkness to reveal ecosystem respiration, R&lt;sub&gt;e&lt;/sub&gt;. Shading was implemented using hoods made of single- and double-layer white mosquito nets while darkness was obtained by covering the chamber with an opaque white hood. The chamber was vented before each measurement and placed carefully on top of the study plot so that the leakage of air from beneath the chamber was minimized. Photosynthetically active radiation (PAR) within the chamber was recorded using an HD 9021 Quantum-Photo-Radiometer. The CO&lt;sub&gt;2&lt;/sub&gt; concentration, temperature, and humidity within chambers were logged at 5-s intervals for 90 s. The CO&lt;sub&gt;2&lt;/sub&gt; flux was calculated using CO&lt;sub&gt;2&lt;/sub&gt; and the chamber microclimate data and corrected for changes in temperature and water vapor pressure (Hooper et al., 2002). The net CO&lt;sub&gt;2&lt;/sub&gt; flux with light intensity above zero was regarded as NEE. For NEE, negative fluxes indicate a net uptake of CO&lt;sub&gt;2&lt;/sub&gt; from the atmosphere, whereas positive fluxes indicate a net release of CO&lt;sub&gt;2&lt;/sub&gt; into the atmosphere. &lt;/span&gt;&lt;/p&gt; &lt;p class="MsoNormal"&gt;&lt;span&gt;For the comparison of daily CO&lt;sub&gt;2&lt;/sub&gt; flux measurements between the treatments and control plots we normalized GPP to the PAR level of 600 µmol m&lt;sup&gt;-2&lt;/sup&gt; s&lt;sup&gt;-1&lt;/sup&gt;. The GPP was calculated from the NEE and R&lt;sub&gt;e&lt;/sub&gt; as:&lt;/span&gt;&lt;/p&gt; &lt;p class="MsoNormal"&gt;&lt;span&gt;GPP = NEE - R&lt;sub&gt;e&lt;/sub&gt;&lt;/span&gt;&lt;/p&gt; &lt;p class="MsoNormal"&gt;&lt;span&gt;Daily plot-specific GPP values were fitted to their corresponding PAR levels using the nonlinear least squares (nls) function from stats package in R software environment  as:&lt;/span&gt;&lt;/p&gt; &lt;p class="MsoNormal"&gt;&lt;span&gt;GPPij = A&lt;sub&gt;max&lt;/sub&gt;PAR / k + PAR&lt;/span&gt;&lt;/p&gt; &lt;p class="MsoNormal"&gt;&lt;span&gt;where i stands for i&lt;sup&gt;th&lt;/sup&gt; plot and j for j&lt;sup&gt;th&lt;/sup&gt; date, A&lt;sub&gt;max&lt;/sub&gt; is the maximum GPP rate when saturated to light (mg CO&lt;sub&gt;2&lt;/sub&gt; m&lt;sup&gt;−2&lt;/sup&gt; h&lt;sup&gt;−1&lt;/sup&gt;) and k is the half-saturation light constant (μmol m&lt;sup&gt;−2&lt;/sup&gt; s&lt;sup&gt;−1&lt;/sup&gt;). Subsequently, the GPP&lt;sub&gt;600&lt;/sub&gt; was calculated for each plot and day at the light level of 600 μmol m&lt;sup&gt;−2&lt;/sup&gt; s&lt;sup&gt;−1&lt;/sup&gt; using Eq. 2 with PAR set to 600.&lt;/span&gt;&lt;/p&gt

Higher vascular plant abundance associated with decreased ecosystem respiration after 20 years of warming in the forest–tundra ecotone

The on-going climate warming is promoting shrub abundance in high latitudes, but the effect of this phenomenon on ecosystem functioning is expected to depend on whether deciduous or evergreen species increase in response to warming. To explore effects of long-term warming on shrubs and further on ecosystem functioning, we analysed vegetation and ecosystem CO2 exchange after 20 years of warming in the forest–tundra ecotone in subarctic Sweden. A previous study conducted 9 years earlier had found increased evergreen Empetrum nigrum ssp. hermaphroditum in the forest and increased deciduous Betula nana in the tundra. Following current understanding, we expected continued increase in shrub abundance that would be stronger in tundra than in forest. We expected warming to increase ecosystem respiration (Re) and gross primary productivity (GPP), with a greater increase in Re in tundra due to increased deciduous shrub abundance, leading to a less negative net ecosystem exchange and reduced ecosystem C sink strength. As predicted, vascular plant abundances were higher in the warmed plots with a stronger response in tundra than in forest. However, whereas B. nana had increased in abundance since the last survey, E. hermaphroditum abundance had declined due to several moth and rodent outbreaks during the past decade. In contrast to predictions, Re was significantly lower in the warmed plots irrespective of habitat, and GPP increased marginally only in the forest. The lower Re and a higher GPP under warming in the forest together led to increased net C sink. Re was negatively associated with the total vascular plant abundance. Our results highlight the importance of disturbance regimes for vegetation responses to warming. Climate warming may promote species with both a high capacity to grow under warmer conditions and a resilience towards herbivore outbreaks. Negative correlation between Re and total vascular plant abundance further indicate that the indirect impacts of increased plants on soil microclimate may become increasingly important for ecosystem CO2 exchange in the long run, which adds to the different mechanisms that link warming and CO2 fluxes in northern ecosystems. Read the free Plain Language Summary for this article on the Journal blog

Decreased soil microbial nitrogen under vegetation 'shrubification' in the subarctic forest–tundra ecotone : the potential role of increasing nutrient competition between plants and soil microorganisms

The consequences of warming-induced ‘shrubification’ on Arctic soil carbon storage are receiving increased attention, as the majority of ecosystem carbon in these systems is stored in soils. Soil carbon cycles in these ecosystems are usually tightly coupled with nitrogen availability. Soil microbial responses to ‘shrubification’ may depend on the traits of the shrub species that increase in response to warming. Increase in deciduous shrubs such as Betula nana likely promotes a loss of soil carbon, whereas the opposite may be true if evergreen shrubs such as Empetrum hermaphroditum increase. We analyzed soil organic matter stocks and 13C NMR fractions, microbial CO2 respiration, biomass, extracellular enzyme activities (EEAs), and their association with shrub density in northern Sweden after 20 years of experimental warming using open top chambers (OTCs). Our study sites were located in a tundra heath that stores high soil carbon quantities and where the OTCs had increased deciduous shrubs, and in a mountain birch forest that stores lower soil carbon quantities and where the OTCs had increased evergreen shrubs. We predicted that organic matter stocks should be lower and respiration and EEAs higher inside the OTCs than untreated plots in the tundra, whereas no effect should be detected in the forest. Soil organic matter stocks and 13C NMR fractions remained unaffected at both sites. When expressed as per gram microbial biomass, respiration and EEAs for carbohydrate and chitin degradation were higher inside the OTCs, and contrasting our prediction, this effect was stronger in the forest. Unexpectedly, the OTCs also led to a substantially lower microbial biomass carbon and nitrogen irrespective of habitat. The decline in the microbial biomass counteracted increased activities resulting in no effect of the OTCs on respiration and a lower phenol oxidase activity per gram soil. Microbial biomass nitrogen correlated negatively with evergreen shrub density at both sites, indicating that ‘shrubification’ may have intensified nutrient competition between plants and soil microorganisms. Nutrient limitation could also underlie increased respiration per gram microbial biomass through limiting C assimilation into biomass. We hypothesize that increasing nutrient immobilization into long-lived evergreen shrubs could over time induce microbial nutrient limitation that contributes to a stability of accumulated soil organic matter stocks under climate warming