How does temperature affect forest “fungus breath”? Diurnal non-exponential temperature-respiration relationship, and possible longer-term acclimation in fungal sporocarps

Abstract

Fungal respiration contributes substantially to ecosystem respiration, yet its field temperature response is poorly characterized. I hypothesized that at diurnal time scales, temperature-respiration relationships would be better described by unimodal than exponential models, and at longer time scales both Q₁₀ and mass-specific respiration at 10 °C (R_ms10) would show signs of acclimation. I measured respiration on intact sporocarps over the course of several days, and modeled temperature-respiration relationships using exponential and unimodal Gaussian functions. Unimodal models provided a better fit than exponential models. R_ms10 and Q₁₀ also declined with increasing temperature, consistent with longer-term temperature acclimation. There was some evidence of diurnal hysteresis. When exponential models were appropriate, Q₁₀ values averaged ∼3.5, and R_ms10 averaged 0.02 μmol CO₂ g⁻¹ sec⁻¹. The observed high mass-specific respiration rates, peaked temperature responses, decline in R_ms10 and Q₁₀ with increasing temperature, and hysteresis could contribute to observed non-exponential and hysteretic patterns in soil and ecosystem respiration.

Introduction

Fungal contributions to ecosystem respiration could be large, yet are poorly constrained. Assuming (1) 10–25% of microbial biomass is fungal (Fierer et al., 2009), (2) microbial biomass is about 4% of root biomass (Fierer et al., 2009), (3) fungal mass-specific respiration is 10× higher than fine roots (e.g., Andrew et al., 2014), (4) fine roots mass-specific respiration is about 3–10× coarse roots (Desrochers et al., 2002, Chen et al., 2010), and (5) fine roots are about 14% of total root mass (Jackson et al., 1997), then soil fungal respiration would equal from 11 to 86% of total root respiration on a per area basis. This back-of-the-envelope calculation makes it clear that fungal respiration could be a major contributor to ecosystem respiration, and hence could play a very important role in the terrestrial C cycle and global climate. It is, therefore, surprising how poorly we understand rates and environmental regulation of fungal respiration, especially given the need to accurately model potential ecosystem feedbacks to climate change.

The effect of temperature on ecosystem respiration is still not fully understood, with efforts focused on quantifying the effects on whole-ecosystem respiration (e.g., Janssens et al., 2001) and two major components— plant respiration (e.g., Ryan, 1991, Atkin and Tjoelker, 2003) and soil respiration (e.g., Lloyd and Taylor, 1994, Davidson and Janssens, 2006), both of which typically include poorly constrained fungal components. This lack of clear partitioning arises from a variety of factors, not the least of which is that partitioning of respiration between autotrophs and heterotrophs can be quite difficult (Hanson et al., 2000). Soil respiration is produced by a combination of broadly defined autotrophic and heterotrophic components. These are often operationally distinguished as autotrophic organisms and their symbiome, i.e., roots plus endorhizal and rhizoplane mycorrhizal, commensal and parasitic fungi and bacteria, as well as mycorrhizosphere organisms that consume exudates; and free-living heterotrophs that consume tissues (mostly saprotrophic and predatory biotrophic organisms). Although less commonly discussed, ‘plant’ respiration also contains fungal respiration, especially in roots because of mycorrhizal associations, but also other plant tissues because of the pervasive presence of fungal endophytes. Given the large differences noted between plant and fungal respiration rates (e.g., Andrew et al., 2014) even a small fungal component could contribute a significant fraction of empirical measurements of plant respiration. In addition it is likely that patterns of plant and fungal respiration respond differently to environmental cues such as temperature and moisture. Therefore, understanding controls on fungal respiration will enhance our ability to model plant symbiotic, soil and ecosystem respiration.

Temperature effects on respiration are sometimes simplistically modeled using Q₁₀ values that specify an exponential rate of change in respiration as a function of temperature. For a variety of reasons we expect Q₁₀ to be insufficient to adequately describe in situ field temperature responses of fungal respiration, as has previously been observed for soil respiration (Lloyd and Taylor, 1994, Davidson et al., 2006, Tuomi et al., 2008). First, we know that exponential rates of change in respiration are only valid over a narrow temperature range, beyond which organelle membranes, enzymes and other cellular constituents function poorly or break down entirely (Tansey and Brock, 1972, Robinson, 2001). Second, the conceptual basis for Q₁₀ is that enzyme kinetics regulate cellular metabolism and should respond exponentially to temperature, yet we know that metabolism is more complex, because it is sensitive to environmental cues that can rapidly up- or down-regulate gene expression, enzyme production, and cellular metabolism (Davidson et al., 2006). Thus, specific biochemical and physiological responses to environmental cues could cause significant deviation from fixed Q₁₀ responses to environmental stimuli such as temperature. Over the long term these could contribute to acclimation responses (Atkin and Tjoelker, 2003, Malcolm et al., 2008), but over the short-term these could result in non-exponential responses to temperature, or variation in Q₁₀ values. Given that fungal tissues are often exposed to widely fluctuating temperatures over diurnal cycles, cellular physiology will be continually responding to these dynamic conditions, potentially leading to more complex response functions. Third, temperature often cycles strongly diurnally, and circadian and other endogenous rhythms can be superimposed on these diurnal cycles (Smith, 1973), potentially altering apparent temperature responses. Fourth, carbon supply can vary as a function of C fixation, transport, and competition with plant sinks, so respiration of mycorrhizal fungi could be linked to cyclic variation or trends in substrate supply (Heinemeyer et al., 2006, Heinemeyer et al., 2012, Kuzyakov and Gavrichkova, 2010). Fifth, water availability can also vary as a function of evaporative losses, hydraulic redistribution and plant sinks (Lilleskov et al., 2009), so respiration responses to temperature could be dampened as a function of diurnal cycles or trends in water availability.

Studies of respiration in the field are either destructive (e.g., Andrew et al., 2014) or non-destructive (e.g., Heinemeyer et al., 2006, Heinemeyer et al., 2007, Heinemeyer et al., 2012). The former provide the opportunity to determine time-point estimates of mass-specific rates of respiration of soil hyphae, which can be useful for scaling based on biomass estimates. They also permit a rapid snapshot of respiration temperature relationships for a large number of individual samples with little time investment. By contrast, the latter provide greater insights into temporal variation in respiration within an in situ organism or community—e.g., as a function of temperature, moisture, and substrate supply—and can be combined with terminal destructive harvests to provide information on mass-specific respiration.

Targets of respiration research include vegetative mycelia (e.g., Heinemeyer et al., 2006, Heinemeyer et al., 2007) and fungal sporocarps (Andrew et al., 2014). Although the former are targets of many recent studies on soil respiration, and represent the majority of fungal biomass in soils (e.g., Wallander et al., 2001), the advantages of the latter are several. First, they provide an opportunity to examine isolated fungal tissues with high biomass per unit area, enabling better estimates of fungal respiratory parameters. Second, the respiration rate can be linked to a species, enabling better estimates of taxon-specific fungal C costs for different functional classes of organisms (e.g., saprotrophs, ectomycorrhizal fungi). Third, understanding the respiratory costs of reproduction is essential to quantifying parameters of fungal carbon balance and fitness. Fourth, our previous work suggests that mass-specific respiration rates are fairly similar between vegetative mycelium and sporocarps (Andrew et al., 2014).

Remarkably, to my knowledge no studies have non-destructively examined sporocarp temperature-respiration relationships in situ. To fill this gap, I designed a custom chamber for examining in situ sporocarp respiration. My goals were to determine whether this system would provide robust estimates of diurnal sporocarp respiration-temperature relationships, to explore whether exponential or unimodal relationships are better for characterizing these relationships, and to begin to accumulate species-specific and functional group estimates of respiration of mycorrhizal and saprotrophic fungi. I hypothesized that (H1) under higher temperatures sporocarp respiration-temperature relationships would deviate downward from a simple exponential Q₁₀, and Gaussian regressions would be better than exponential regressions at representing these relationships; (H2) when approaching freezing temperatures, respiration would exhibit upward deviations from exponential relationships consistent with metabolic responses to cold stress; and (H3) when comparing sporocarps growing at different temperatures respiration would decline with increasing temperature, consistent with acclimation responses. Additionally I compare respiration estimates with published estimates for tree fine roots in order to begin to provide some additional insight into relative root and fungal contributions to soil respiration.