Author Posting. © The Author(s), 2009.  This is the author's version of the work. It is posted here by permission of Blackwell for personal use, not for redistribution.  The definitive version was published in Ecology Letters 12 (2009): E15-E18, doi:10.1111/j.1461-0248.2009.01332.x.Hartley et al. question whether reduction in Rmass, under experimental warming, arises because of
the biomass method. We show the method they treat as independent yields the same result. We
describe why the substrate-depletion hypothesis cannot alone explain observed responses, and
urge caution in the interpretation of the seasonal data.This research was supported by the Office of Science (BER), U.S. Department of Energy, the
Andrew W. Mellon Foundation and U.S. National Science Foundation grants to the Coweeta
LTER program

Allison, Steven D.

Bradford, Mark A.

Davies, Christian A.

Frey, Serita D.

Maddox, Thomas R.

Melillo, Jerry M.

Mohan, Jacqueline E.

Reynolds, James F.

Treseder, Kathleen K.

Wallenstein, Matthew D.

Watts, Brian W.

English

Woods Hole Open Access Server

Bradford et al. 1Decreased mass specific respiration under experimental warming is 1 robust to the microbial biomass method employed  2 Mark A. Bradford,1* Matthew D. Wallenstein,2 Steven D. Allison,3 Kathleen K. Treseder,3 3 Serita D. Frey,4 Brian W. Watts,5 Christian A. Davies,5 Thomas R. Maddox,5 Jerry M. 4 Melillo,6 Jacqueline E. Mohan5 and James F. Reynolds7 5 1School of Forestry and Environmental Studies, Yale University, New Haven, CT 06511, USA 6 2Natural Resource Ecology Laboratory, Colorado State University, Fort Collins, CO 80523, 7 USA  8 3Ecology & Evolutionary Biology, University of California, Irvine, CA 92697, USA 9 4Department of Natural Resources, University of New Hampshire, Durham, NH 03824, USA 10 5Odum School of Ecology, University of Georgia, Athens, GA 30602, USA  11 6The Ecosystems Center, Marine Biological Laboratory, Woods Hole, MA 02543, USA 12 7Nicholas School of the Environment and Earth Sciences, and Department of Biology, Duke 13 University, Durham, NC 27708, USA 14 Author e-mails: mark.bradford@yale.edu, mawallen@nrel.colostate.edu, allisons@uci.edu, 15 treseder@uci.edu, serita.frey@unh.edu, booralun@uga.edu, drcadavies@gmail.com, 16 trmaddox@uga.edu, jmelillo@mbl.edu, jmohan@uga.edu, james.f.reynolds@duke.edu 17 Keywords: Acclimation, adaptation, soil respiration, thermal biology, temperature, carbon 18 cycling, climate change, climate warming, microbial community, CO2 19 Type of article: Technical comment 20 Abstract 50 words; manuscript 788 words; 15 references; 2 figures; *mailing and e-mail address 21 of Mark A. Bradford is as above; tel. +1 203 436 9148, fax. +1 203 432 3929 22 Bradford et al. 2Abstract 23 Hartley et al. question whether reduction in Rmass, under experimental warming, arises because of 24 the biomass method. We show the method they treat as independent yields the same result. We 25 describe why the substrate-depletion hypothesis cannot alone explain observed responses, and 26 urge caution in the interpretation of the seasonal data. 27  28 Keywords 29 Acclimation, adaptation, soil respiration, thermal biology, temperature, carbon cycling, climate 30 change, climate warming, microbial biomass, CO2 31  32 33 Bradford et al. 3Hartley et al. (2009) make two important observations on our work (Bradford et al. 2008) and re-34 analyse our seasonal data. We respond to each observation and then discuss the re-analysis. 35  The first observation is that we calculated Rmass as a ratio between two respiration-based 36 measures. The positive relationship between these two variables, and importantly the negative 37 intercept, means that as SIR biomass increases Rmass follows a positive hyperbolic function. 38 Specifically, across higher biomass values (in the organic horizon) there is little change in Rmass 39 but at lower biomass values (in the mineral horizon) Rmass co-varies markedly. Had the intercept 40 between sucrose respiration and SIR biomass been zero then Rmass would have been constant; had 41 it been positive then Rmass would have decreased as biomass increased. Hartley et al. (2009) 42 present their seasonal re-analysis (see below) using CFE microbial biomass; they consider it a 43 more independent measure. If we calculate Rmass using CFE then we observe that under 44 experimental warming Rmass is reduced (Fig. 1). That is, our observation that prolonged 45 experimental warming decreases Rmass is robust to the microbial biomass method employed. 46  The second observation is that if our method to calculate Rmass is appropriate, the lower 47 Rmass is more likely due to a depletion in labile carbon, rather than thermal adaptation. From this 48 Hartley et al. (2009) conclude that the substrate-depletion hypothesis most likely explains the 49 ephemeral augmentation of respiration in warming experiments. We agree that substrate-50 depletion likely contributes to this augmentation and present the first field evidence that labile 51 carbon pools decline in response to experimental warming (see Bradford et al. 2008). However, 52 the substrate-depletion hypothesis does not make explicit predictions about microbial biomass or 53 Rmass (Kirschbaum 2004; Eliasson et al. 2005; Knorr et al. 2005); no change in microbial 54 metabolism or carbon supply is invoked to explain respiration dynamics (see Kirschbaum 2004). 55 This makes inferences from the hypothesis about microbial biomass and activity responses 56 Bradford et al. 4speculative. For example, the depletion of labile carbon pools does not imply that microbial 57 biomass should decline due to carbon limitation, since the substrate-depletion hypothesis 58 assumes equal carbon supply in control and heated soils at equilibrium. This led us (Bradford et 59 al. 2008) to speculate that decreased root-carbon supply could explain the microbial biomass 60 decreases we observed under experimental warming. Decreases could also have arisen through 61 reduced carbon-use efficiencies (Steinweg et al. 2008), altered growth rates (Bárcenas-Moreno et 62 al. 2009), and/or shifts in microbial community composition in the plots (Frey et al. 2008). 63 Whether depletion of labile carbon pools drives any of these changes is currently unclear. 64 Nonetheless, the substrate-depletion hypothesis cannot solely explain observed responses of soil 65 microbes and their respiration to warming; nor was it presented as a panacea (see Kirschbaum 66 2004). The soil and global change communities need to focus more attention on microbial and 67 plant responses when explaining soil respiration responses to warming. 68  In their re-analysis of our seasonal data, Hartley et al. (2009) suggest there is evidence 69 for thermal adaptation enhancing the response of soil microbial respiration to warming. We 70 acknowledge their conclusion but suggest that perhaps we and Hartley et al. (2009) over-stepped 71 what could be concluded about Rmass responses to seasonal temperature change using the SIR and 72 CFE methods, respectively. Although CFE and SIR share a common origin (Anderson & 73 Domsch 1978; Vance et al. 1987; Jenkinson et al. 2004), and yield biomass estimates that are 74 correlated (Wardle & Parkinson 1991; Anderson & Joergensen 1997), they both have limitations. 75 First, they provide ‘estimates’ of biomass. We relied on SIR because it is more effective at 76 resolving active biomass differences at plot-scales (Wardle & Ghani 1995); CFE is often poor for 77 detecting fine-scale variation. After finding approximately equivalent experimental-warming 78 responses using both methods (Fig. 1 and Bradford et al. 2008), we proceeded to the seasonal 79 Bradford et al. 5analysis using only SIR. Yet, Hartley et al.’s (2009) re-analysis highlights how this affects our 80 interpretation of the seasonal data (Fig. 2). There is clearly a need for development of 81 methodology to provide robust, fine-scale, independent measures of microbial biomass. In the 82 absence of these, we emphasize the seasonal patterns that are independent of the biomass 83 method, and even biomass correction. Particularly pronounced is the seasonal shift in the shape 84 of the temperature response, suggesting the optimum is shifted to the right in the warm season 85 (Fig. 2a-c). In addition, sucrose respiration rates for each season diverge markedly across the 86 temperature range (Fig. 2), highlighting the importance of considering biomass changes. These 87 patterns are obscured for soil respiration (Fig. 2). This may mean that soil respiration responses 88 to warming can mask marked shifts in microbial biomass and temperature response of microbial 89 respiration. We conclude that the relative roles and interactions of substrate-depletion versus 90 microbial responses remain unresolved in warming soils. 91  92 ACKNOWLEDGEMENTS 93 This research was supported by the Office of Science (BER), U.S. Department of Energy, the 94 Andrew W. Mellon Foundation and U.S. National Science Foundation grants to the Coweeta 95 LTER program. We thank four anonymous reviewers, the editors and Iain Hartley and Phil 96 Wookey for constructive comments.  97  98 REFERENCES 99 Anderson J.P.E. & Domsch K.H. (1978). A physiological method for the quantitative 100 measurement of microbial biomass in soils. Soil Biol. Biochem., 10, 215-221. 101 Bradford et al. 6Anderson T.-H. & Joergensen R.G. (1997). Relationship between SIR and FE estimates of 102 microbial biomass C in deciduous forest soils at different pH. Soil Biol. Biochem., 29, 103 1033-1042. 104 Bárcenas-Moreno G., Gómez-Brandón M., Rousk J. & Bååth E. (2009). Adaptation of soil 105 microbial communities to temperature: comparison of fungi and bacteria in a laboratory 106 experiment. Global Change Biol., doi: 10.1111/j.1365-2486.2009.01882.x. 107 Bradford M.A., Davies C.A., Frey S.D., Maddox T.R., Mohan J.M., Reynolds J.F., Treseder 108 K.K. & Wallenstein M.D. (2008). Thermal adaptation of soil microbial respiration to 109 elevated temperature. Ecol. Lett., 11, 1316-1327. 110 Eliasson P.E., McMurtrie R.E., Pepper D.A., Strömgren M., Linder S. & Ågren G.I. (2005). The 111 response of heterotrophic CO2 flux to soil warming. Global Change Biol., 11, 167-181. 112 Fenner N., Freeman C. & Reynolds B. (2005). Observations of a seasonally shifting thermal 113 optimum in peatland carbon-cycling processes; implications for the global carbon cycle 114 and soil enzyme methodologies. Soil Biol. Biochem., 37, 1814-1821. 115 Frey S.D., Drijber R., Smith H. & Melillo J. (2008). Microbial biomass, functional capacity, and 116 community structure after 12 years of soil warming Soil Biol. Biochem., 40, 2904-2907. 117 Hartley I.P., Hopkins D.W., Garnett M.H., Sommerkorn M. & Wookey P.A. (2009). No 118 evidence for compensatory thermal adaptation of soil microbial respiration in the study of 119 Bradford et al. (Ecol. Lett., 2008, 11, 1316-1327). Ecol. Lett., in press. 120 Jenkinson D.S., Brookes P.C. & Powlson D.S. (2004). Measuring soil microbial biomass. Soil 121 Biol. Biochem., 36, 5-7. 122 Kirschbaum M.U.F. (2004). Soil respiration under prolonged soil warming: are rate reductions 123 caused by acclimation or substrate loss? Global Change Biol., 10, 1870-1877. 124 Bradford et al. 7Knorr W., Prentice I.C., House J.I. & Holland E.A. (2005). Long-term sensitivity of soil carbon 125 turnover to warming. Nature, 433, 298-301. 126 Steinweg J.M., Plante A.F., Conant R.T., Paul E.A. & Tanaka D.L. (2008). Patterns of substrate 127 utilization during long-term incubations at different temperatures. Soil Biol. Biochem., 128 40, 2722-2728. 129 Vance E.D., Brookes P.C. & Jenkinson D.S. (1987). An extraction method for measuring soil 130 microbial biomass C. Soil Biol. Biochem., 19, 703-707. 131 Wardle D.A. & Ghani A. (1995). Why is the strength of relationships between pairs of methods 132 for estimating soil microbial biomass often so variable? Soil Biol. Biochem., 27, 821-828. 133 Wardle D.A. & Parkinson D. (1991). A statistical evaluation of equations for predicting total 134 microbial biomass carbon using physiological and biochemical methods. Agr. Ecosyst. 135 Environ., 34, 75-86. 136  137 138 Bradford et al. 8Figure  1  Rates of soil microbial respiration of sucrose, expressed per unit CFE microbial 139 biomass, in control and heated soils at three measurement temperatures. These plots are 140 equivalent to Fig. S4 in Bradford et al. (2008) excepting that in the original figure rates of 141 sucrose respiration are expressed per unit SIR microbial biomass. Field soils were sampled from 142 control (closed circles) and heated (open circles) plots (n = 6) and then assayed to assess sucrose 143 mineralization rates across a temperature range from 10 to 20C, and biomass using the CFE 144 method (for details see Bradford et al. 2008). Shown are data from assays performed for the 145 upper mineral soil horizon across early spring (April) to late fall (November). The observed 146 pattern is that Rmass is generally lower, at a specific measurement temperature, following long-147 term, experimental warming. Values are means  1 s.e.m., n = 6. Given that Rmass is essentially a 148 ratio, note that standard errors were propagated from the errors in the microbial biomass and 149 sucrose respiration data. This same pattern was observed with the SIR biomass corrected data 150 (see Bradford et al. 2008). 151  152 Figure  2  Respiration rates of soils sampled in the cool and warm seasons at three measurement 153 temperatures, following the approach of Hartley et al. (2009). Note that this approach pools 154 across the experimental treatments and soil horizons. Therefore the patterns observed in Fig. 1 do 155 not relate to what is shown in this figure. In their re-analysis of our seasonal data using CFE 156 microbial biomass, Hartley et al. (2009) conclude that the large increase in Rmass rates at 157 measurement temperatures of 20C, for soils sampled in the warm season (a), implies that 158 thermal adaptation will enhance the response of soil microbial respiration to persistent warming. 159 A different interpretation is obtained if one uses SIR estimates of biomass to calculate Rmass rates 160 (b). There are potentially issues with both of these approaches. Indeed, mean daily temperature 161 Bradford et al. 9across the preceding 9 or 11 weeks explained 64 and 75% of the seasonal variation in Rmass 162 (based on SIR) for the organic and mineral horizons, respectively (see Bradford et al. 2008). 163 However, the same analysis using CFE biomass to calculate Rmass explained no significant 164 variation (r2 values <0.01; showing less than 1% of variance explained). This may be because 165 CFE biomass values are highly variable at fine-spatial scales compared to SIR biomass estimates 166 (see text for additional discussion). However, the apparent seasonal shift in the thermal optimum 167 for Rmass appears independent of the biomass method employed (a,b), and is also observed if 168 sucrose respiration data are not corrected for biomass (c). That is, that rates in cool season soils 169 increase markedly between measurement temperatures of 10 and 15C, and little between 15 and 170 20C, whereas the opposite pattern is observed for warm season soils (a-c). That thermal optima 171 for Rmass rates track seasonal temperature corresponds with similar tracking of other microbial 172 activities involving carbon degradation (Fenner et al. 2005) and is a consistent pattern in our 173 seasonal dataset. Notably, the pattern is not observed for soil respiration, expressed where 174 substrate-limitation has not been alleviated, and without correction for biomass (d and see text). 175 Bradford et al. 10Fig. 1 176 177 Bradford et al. 11Fig. 2 178  179 

Decreased mass specific respiration under experimental warming is robust to the microbial biomass method employed

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Decreased mass specific respiration under experimental warming is robust to the microbial biomass method employed

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