Herbivore diversity effects on Arctic tundra ecosystems: a systematic review

Background: Northern ecosystems are strongly influenced by herbivores that differ in their impacts on the ecosystem. Yet the role of herbivore diversity in shaping the structure and functioning of tundra ecosystems has been overlooked. With climate and land-use changes causing rapid shifts in Arctic species assemblages, a better understanding of the consequences of herbivore diversity changes for tundra ecosystem functioning is urgently needed. This systematic review synthesizes available evidence on the effects of herbivore diversity on different processes, functions, and properties of tundra ecosystems. Methods: Following a published protocol, our systematic review combined primary field studies retrieved from bibliographic databases, search engines and specialist websites that compared tundra ecosystem responses to different levels of vertebrate and invertebrate herbivore diversity. We used the number of functional groups of herbivores (i.e., functional group richness) as a measure of the diversity of the herbivore assemblage. We screened titles, abstracts, and full texts of studies using pre-defined eligibility criteria. We critically appraised the validity of the studies, tested the influence of different moderators, and conducted sensitivity analyses. Quantitative synthesis (i.e., calculation of effect sizes) was performed for ecosystem responses reported by at least five articles and meta-regressions including the effects of potential modifiers for those reported by at least 10 articles. Review findings: The literature searches retrieved 5944 articles. After screening titles, abstracts, and full texts, 201 articles including 3713 studies (i.e., individual comparisons) were deemed relevant for the systematic review, with 2844 of these studies included in quantitative syntheses. The available evidence base on the effects of herbivore diversity on tundra ecosystems is concentrated around well-established research locations and focuses mainly on the impacts of vertebrate herbivores on vegetation. Overall, greater herbivore diversity led to increased abundance of feeding marks by herbivores and soil temperature, and to reduced total abundance of plants, graminoids, forbs, and litter, plant leaf size, plant height, and moss depth, but the effects of herbivore diversity were difficult to tease apart from those of excluding vertebrate herbivores. The effects of different functional groups of herbivores on graminoid and lichen abundance compensated each other, leading to no net effects when herbivore effects were combined. In turn, smaller herbivores and large-bodied herbivores only reduced plant height when occurring together but not when occurring separately. Greater herbivore diversity increased plant diversity in graminoid tundra but not in other habitat types. Conclusions: This systematic review underscores the importance of herbivore diversity in shaping the structure and function of Arctic ecosystems, with different functional groups of herbivores exerting additive or compensatory effects that can be modulated by environmental conditions. Still, many challenges remain to fully understand the complex impacts of herbivore diversity on tundra ecosystems. Future studies should explicitly address the role of herbivore diversity beyond presence-absence, targeting a broader range of ecosystem responses and explicitly including invertebrate herbivores. A better understanding of the role of herbivore diversity will enhance our ability to predict whether and where shifts in herbivore assemblages might mitigate or further amplify the impacts of environmental change on Arctic ecosystems

Location of studies and evidence of effects of herbivory on Arctic vegetation: a systematic map

Herbivores modify the structure and function of tundra ecosystems. Understanding their impacts is necessary to assess the responses of these ecosystems to ongoing environmental changes. However, the effects of herbivores on plants and ecosystem structure and function vary across the Arctic. Strong spatial variation in herbivore effects implies that the results of individual studies on herbivory depend on local conditions, i.e., their ecological context. An important first step in assessing whether generalizable conclusions can be produced is to identify the existing studies and assess how well they cover the underlying environmental conditions across the Arctic. This systematic map aims to identify the ecological contexts in which herbivore impacts on vegetation have been studied in the Arctic. Specifically, the primary question of the systematic map was: “What evidence exists on the effects of herbivores on Arctic vegetation?”

Climate and forest properties explain wildfire impact on microbial community and nutrient mobilization in boreal soil

The boreal landscape stores an estimated 40% of the earth's carbon (C) found in terrestrial vegetation and soils, with a large portion collected in thick organic soil layers. These ground stores are subject to substantial removals due to the centurial return of wildfire, which has strong impacts on the soil microbial community and nutrient cycling, which in turn can control ecosystem recovery patterns and process rates, such as C turnover. Currently, predictive knowledge used in assessing fire impacts is largely focused on ecosystems that experience only superficial burning and few robust observations exist regarding the effect that smoldering combustion in deeper active soil layers has on post-fire soil activity. This study provided a highly replicated and regionally extensive survey of wildfire impact on microbial community structure (using fatty acid biomarkers) and nutrient cycling (using in situ ionic resin capsules) across broad gradients of climate, forest properties and fire conditions within 50 separate burn scars and 50 additional matched unburnt boreal forest soils. The results suggest a strong metabolic shift in burnt soils due to heat impact on their structure and a decoupling from aboveground processes, releasing ecosystem N limitation and increasing mobilization of N, P, K, and S as excess in conjunction with an altered, C-starved microbial community structure and reduced root uptake due to vegetation mortality. An additional observed climatic control over burnt soil properties has implications for altered boreal forest function in future climate and fire regimes deserving of further attention

Climatic variation drives loss and restructuring of carbon and nitrogen in boreal forest wildfire

The boreal forest landscape covers approximately 10% of the earth's land area and accounts for almost 30 % of the global annual terrestrial sink of carbon (C). Increased emissions due to climate-change-amplified fire frequency, size, and intensity threaten to remove elements such as C and nitrogen (N) from forest soil and vegetation at rates faster than they accumulate. This may result in large areas within the region becoming a net source of greenhouse gases, creating a positive feedback loop with a changing climate. Meter-scale estimates of area-normalized fire emissions are limited in Eurasian boreal forests, and knowledge of their relation to climate and ecosystem properties is sparse. This study sampled 50 separate Swedish wildfires, which occurred during an extreme fire season in 2018, providing quantitative estimates of C and N loss due to fire along a climate gradient. Mean annual precipitation had strong positive effects on total fuel, which was the strongest driver for increasing C and N losses. Mean annual temperature (MAT) influenced both pre-and postfire organic layer soil bulk density and C: N ratio, which had mixed effects on C and N losses. Significant fire-induced loss of C estimated in the 50 plots was comparable to estimates in similar Eurasian forests but approximately a quarter of those found in typically more intense North American boreal wildfires. N loss was insignificant, though a large amount of fire-affected fuel was converted to a low C: N surface layer of char in proportion to increased MAT. These results reveal large quantitative differences in C and N losses between global regions and their linkage to the broad range of climate conditions within Fennoscandia. A need exists to better incorporate these factors into models to improve estimates of global emissions of C and N due to fire in future climate scenarios. Additionally, this study demonstrated a linkage between climate and the extent of charring of soil fuel and discusses its potential for altering C and N dynamics in postfire recovery

Background insect herbivory increases with local elevation but makes minor contribution to element cycling along natural gradients in the Subarctic

Herbivores can exert major controls over biogeochemical cycling. As invertebrates are highly sensitive to temperature shifts (ectothermal), the abundances of insects in high-latitude systems, where climate warming is rapid, is expected to increase. In subarctic mountain birch forests, research has focussed on geometrid moth outbreaks, while the contribution of background insect herbivory (BIH) to elemental cycling is poorly constrained. In northern Sweden, we estimated BIH along 9 elevational gradients distributed across a gradient in regional elevation, temperature, and precipitation to allow evaluation of consistency in local versus regional variation. We converted foliar loss via BIH to fluxes of C, nitrogen (N), and phosphorus (P) from the birch canopy to the soil to compare with other relevant soil inputs of the same elements and assessed different abiotic and biotic drivers of the observed variability. We found that leaf area loss due to BIH was similar to 1.6% on average. This is comparable to estimates from tundra, but considerably lower than ecosystems at lower latitudes. The C, N, and P fluxes from canopy to soil associated with BIH were 1-2 orders of magnitude lower than the soil input from senesced litter and external nutrient sources such as biological N fixation, atmospheric deposition of N, and P weathering estimated from the literature. Despite the minor contribution to overall elemental cycling in subarctic birch forests, the higher quality and earlier timing of the input of herbivore deposits to soils compared to senesced litter may make this contribution disproportionally important for various ecosystem functions. BIH increased significantly with leaf N content as well as local elevation along each transect, yet showed no significant relationship with temperature or humidity, nor the commonly used temperature proxy, absolute elevation. The lack of consistency between the local and regional elevational trends calls for caution when using elevation gradients as climate proxies

The biogeochemical consequences of litter transformation by insect herbivory in the Subarctic : a microcosm simulation experiment

Warming may increase the extent and intensity of insect defoliations within Arctic ecosystems. A thorough understanding of the implications of this for litter decomposition is essential to make predictions of soil-atmosphere carbon (C) feedbacks. Soil nitrogen (N) and C cycles naturally are interlinked, but we lack a detailed understanding of how insect herbivores impact these cycles. In a laboratory microcosm study, we investigated the growth responses of heterotrophic soil fungi and bacteria as well as C and N mineralisation to simulated defoliator outbreaks (frass addition), long-term increased insect herbivory (litter addition at higher background N-level) and non-outbreak conditions (litter addition only) in soils from a Subarctic birch forest. Larger amounts of the added organic matter were mineralised in the outbreak simulations compared to a normal year; yet, the fungal and bacterial growth rates and biomass were not significantly different. In the simulation of long-term increased herbivory, less litter C was respired per unit mineralised N (C:N of mineralisation decreased to 20 +/- 1 from 38 +/- 3 for pure litter), which suggests a directed microbial mining for N-rich substrates. This was accompanied by higher fungal dominance relative to bacteria and lower total microbial biomass. In conclusion, while a higher fraction of foliar C will be respired by insects and microbes during outbreak years, predicted long-term increases in herbivory linked to climate change may facilitate soil C-accumulation, as less foliar C is respired per unit mineralised N. Further work elucidating animal-plant-soil interactions is needed to improve model predictions of C-sink capacity in high latitude forest ecosystems.Correction: Kristensen, J.A., Metcalfe, D.B., Rousk, J. The biogeochemical consequences of litter transformation by insect herbivory in the Subarctic: a microcosm simulation experiment. Biogeochemistry. 2018;138:337. https://doi.org/10.1007/s10533-018-0451-0</p

Restricted plant diversity limits carbon recapture after wildfire in warming boreal forests

Incomplete wildfire combustion in boreal forests leaves behind legacy plant-soil feedbacks known to restrict plant biodiversity. These restrictions can inhibit carbon recapture after fire by limiting ecosystem transition to vegetation growth patterns that are capable of offsetting warmth-enhanced soil decomposition under climate change. Here, we field-surveyed plant regrowth conditions 2 years after 49 separate, naturally-occurring wildfires spanning the near-entire climatic range of boreal Fennoscandia in order to determine the local to regional scale drivers of early vegetation recovery. Minimal conifer reestablishment was found across a broad range of fire severities, though residual organic soil and plant structure was associated with restricted growth of a variety of more warmth-adapted vegetation, such as broadleaf trees. This dual regeneration limitation coincided with greater concentrations of bacterial decomposers in the soil under increased mean annual temperature, potentially enhancing soil carbon release. These results suggest that large portions of the boreal region are currently at risk of extending postfire periods of net emissions of carbon to the atmosphere under limitations in plant biodiversity generated by wildfire and a changing climate

Mineral soils are an important intermediate storage pool of black carbon in fennoscandian boreal forests

Approximately 40% of earth's carbon (C) stored in land vegetation and soil is within the boreal region. This large C pool is subjected to substantial removals and transformations during periodic wildfire. Fire-altered C, commonly known as pyrogenic carbon (PyC), plays a significant role in forest ecosystem functioning and composes a considerable fraction of C transport to limnic and oceanic sediments. While PyC stores are beginning to be quantified globally, knowledge is lacking regarding the drivers of their production and transport across ecosystems. This study used the chemo-thermal oxidation at 375°C (CTO-375) method to isolate a particularly refractory subset of PyC compounds, here called black carbon (BC), finding an average increase of 11.6 g BC m−2 at 1 year postfire in 50 separate wildfires occurring in Sweden during 2018. These increases could not be linked to proposed drivers, however BC storage in 50 additional nearby unburnt soils related strongly to soil mass while its proportion of the larger C pool related negatively to soil C:N. Fire approximately doubled BC stocks in the mineral layer but had no significant effect on BC in the organic layer where it was likely produced. Suppressed decomposition rates and low heating during fire in mineral subsoil relative to upper layers suggests potential removals of the doubled mineral layer BC are more likely transported out of the soil system than degraded in situ. Therefore, mineral soils are suggested to be an important storage pool for BC that can buffer short-term (production in fire) and long-term (cross-ecosystem transport) BC cycling