Soil Microbial Responses to Herbivory in an Arctic Tundra Heath at Two Levels of Nutrient Availability

Abstract

We tested the hypothesis that herbivory accelerates nutrient cycling through nutrient‐rich soils and decelerates nutrient cycling through nutrient‐poor soils in a well‐drained arctic tundra heath by measuring effects of herbivory on soil and plant properties in control areas and areas treated with NPK fertilizer. The impact of herbivores was studied with two types of exclosures, one excluding reindeer and the other excluding both rodents and reindeer. We predicted that herbivores would enhance soil microbial processes in the fertilized areas, but retard them in the unfertilized ones. Microbial respiration and microbial C were significantly lower in grazed areas than in herbivore exclosures in both unfertilized and fertilized treatments, indicating that herbivores limit the C available for the soil microbes. Microbial N was significantly increased in the exclosures in the fertilized treatment, but there were no effects in the unfertilized one. This reflects both an increase in resources by fertilization and the effect of herbivores on microbial N acquisition: there was surplus N in the fertilized areas to be immobilized by microbial biomass only when access by herbivores was prevented. Thus, mammalian grazers affect the resource coupling between the plant and microbial trophic levels. Fertilization did not affect the soil inorganic, organic, or microbial N contents, or litter decomposition rates, but it significantly increased soil and microbial P. Microbial C was significantly decreased by fertilization, contradicting some earlier fertilization studies in the arctic. One reason for deceleration of soil nutrient cycling in our study area may be that herbivory by both reindeer and rodents occurs mainly outside the growing season; hence, mammalian waste products do not contribute to soil nutrient availability at the times of highest nutrient demands by plants. In addition, grazing during reindeer migrations is likely to cause net resource output from the system.

Above- and belowground responses to long-term herbivore exclusion

“…Our data show little change from previous samplings, which also show relatively few changes over time (Gough and Johnson 2018), and provide valuable additional time points for this experiment and the examination of ecosystem functions in a changing arctic environment. Interestingly, in a study design similar to ours in another heath community but also including fertilization (Stark and Grellmann 2002), slower nutrient cycling under grazing after seven years of exclusion was reported. Their research found that excluding herbivores influenced MBC and microbial respiration, but MBN was only affected by exclusion plus fertilization (Stark and Grellmann 2002).…”

“…Though these exclosures were monitored for the past twenty years, the impact of herbivore exclusion on soil biogeochemical and physical processes remains unexamined. Furthermore, most studies have focused on the influence of herbivory on arctic vegetation and ecosystem-level processes, and fewer studies have assessed the long-term impacts of arctic herbivores on soil nutrient pools and microbial processes (although see Stark and Grellmann 2002;Olofsson, Stark, and Oksanen 2004;Sitters et al 2017Sitters et al , 2019Stark et al 2019). This has led to the need to have a better understanding of the role of herbivores in systems with slow nutrient cycling.…”

Vertebrate herbivores and ecosystem control: cascading effects of faeces on tundra ecosystems

“…Our findings are in line with reindeer exclusion studies from the Fennoscandian tundra where reindeer grazing appeared to largely enhance nutrient cycling (Stark et al 2002). However, deceleration of soil nutrient cycling was observed in continental sites, where herbivory by both reindeer and rodents occurred largely outside the growing season, perhaps preventing nutrient subsidy from animal waste products at the time of highest nutrient demand in plants and microbes (Stark and Grellmann 2002).…”

“…There is a growing body of evidence, however, indicating that tundra ecosystems are strongly influenced by grazing animals (Manseau et al 1996, Jano et al 1998, Virtanen 2000, Olofsson et al 2001, Van der Wal et al 2001a, b, Stark and Grellmann 2002). These cold systems, which are often dominated by mosses and lichens, were found to be particularly prone to indirect herbivore effects.…”

Carbon storage in terrestrial ecosystems: do browsing and grazing herbivores matter?

“…Over longer periods, soil fertility may play an important role in mediating shifts in plant community composition due to herbivory, which determine the quality of carbon inputs to soils, and consequently, the direction of the responses of microbial communities (Sankaran & Augustine, 2004). Herbivores also influence rates of soil microbial activity and respiration through altering soil temperature and moisture content (Bardgett & Wardle, 2003; Gornall et al , 2007), and this effect varies with air temperature (Sjögersten, van der Wal & Woodin, 2008), seasonal precipitation (Classen et al , 2007), and the seasonal timing of herbivory relative to plant production (Stark & Grellmann, 2002). Finally, herbivores can alter soil respiration by accelerating soil erosion and leaching through reducing plant and standing litter cover, which increases the exposure of the soil surface to precipitation (Wood & Blackburn, 1981).…”