Review PaperTracing S dynamics in agro-ecosystems using 34S
Introduction
There are four stable isotopes of sulfur (32S, 33S, 34S and 36S) with natural isotopic abundances of 0.9499, 0.0075, 0.0425 and 0.0001 atom fraction, respectively (Berglund and Wieser, 2011). Among the three lesser stable isotopes, 34S has been the only one used in tracer studies in terrestrial ecosystems. Three basic types of tracer studies are possible with 34S. An 34S-modified compound such as a fertilizer, either artificially-enriched (e.g. Hamilton et al., 1991, Trivelin et al., 2002) or artificially-depleted (Teixeira et al., 2002) in 34S, can be introduced into the system under study, or alternatively, variations in the natural abundance of 34S in the system S pools can be followed (e.g. Chae and Krouse, 1986, Zhao et al., 2003). While the use of 34S-depletion (D) has been reported in only one study so far, 34S enrichment (E) and 34S natural abundance (NA) have played significant roles in gaining new insight into S cycling in agro-ecosystems.
Compared with other stable isotopes, for example 15N and 13C, 34S has been used to a far lesser extent as a tracer in the biological and agricultural sciences. There are undoubtedly several reasons for this. Firstly, there is a commercially-available radioisotope of S, 35S, which is a low energy β-emitter (0.167 MeV) with a half-life of 87.5 days. Until stricter controls on the use of radioisotopes were imposed in many countries through Occupational Health and Safety regulations, 35S was widely used in research (e.g. Till and May, 1971, Hamilton et al., 1992) since it was cheap, relatively safe to handle with a convenient half-life, and was readily measured by liquid scintillation counting. On the other hand, 34S enriched compounds were not readily available or were extremely expensive, and required a major capital investment of an isotope-ratio mass spectrometer (IRMS). In addition, a major disincentive was the need for manual sample preparation which was tedious and complicated with few samples being processed in one day (e.g. Hamilton et al., 1991).
Compared to nitrogen, sulfur is required by plants in significantly smaller amounts, which is generally reflected in their respective ratio of N: S of approximately 10: 1 in soil organic matter. Although deficiency symptoms of pale yellow foliage are similar, sulfur deficiencies in plants have occurred less frequently than N deficiencies, which may be partly related to one or more of the following; atmospheric deposition from industrial sources (Krouse, 1977, Case and Krouse, 1980, Krouse and Case, 1981); deposition from ocean aerosol (Mizota and Sasaki, 1996, Zazzo et al., 2011); or the widespread use in agriculture of single-superphosphate containing 11–12% S as CaSO4·H2O.
However, the incidence of S deficiency in agro-ecosystems is predicted to increase because single superphosphate is being phased out in favor of so-called high analysis P fertilizers such as triple superphosphate that contain little S (Blair, 2008). Coupled with this trend there have been increased plantings of Brassica crops such as oilseed canola which have a high demand for S. At the same time, S emissions from industrial sources have been reduced worldwide. e.g. in Canada SOx emissions in 2012 were 59% lower than in 1990 (Environment Canada, 2014). Based on a risk assessment model using soil and atmospheric deposition data, McGrath and Zhao (1995) predicted an increased usage of S fertilizers in cereal production in the UK due to continually decreasing inputs of S via atmospheric SO2 accretion.
Although several authors have mentioned the possibility of tracing S dynamics in agro-ecosystems using 34S tracer (e.g. Krouse and Tabatabai, 1986, Giesemann et al., 1995b, Mayer and Krouse, 1996), the majority of studies have occurred in forest ecosystems (Johnson et al., 1986, Alewell and Giesemann, 1996, Novák et al., 2003), including the influence of atmospheric pollution (Krouse and Van Everdingen, 1984). Since forest ecosystem 34S studies have been adequately reviewed elsewhere (e.g. Krouse et al., 1996) they will not be covered here. The distribution of 34S in natural ecosystems may be considered for comparative purposes in the case where few or no data are available for a particular S transformation in an agro-ecosystem. The objective of the present review is to explore the role that 34S has played in tracing the dynamics of S in agro-ecosystems, and to identify future opportunities for exploiting 34S in applied agro-ecosystem research.
Section snippets
Forms and transformations of S in the soil-plant system
A simplified illustration of the S cycle in the soil-plant-atmosphere continuum is depicted in Fig. 1. Sulfur occurs in soils as both inorganic and organic forms. The greater proportion of total S in surface soils is organic S, which is compromised of two forms, carbon bonded S (C-S) and ester sulfate S (R-O-SO3) (Freney, 1986). The most oxidized inorganic form is soluble sulfate (SO42−) and the most reduced form is insoluble sulfide (S2−). Depending on the soil redox potential S may exist in
Absolute (x) and relative (δ) values of 34S abundance
The terminology and conventions for expressing stable isotopic abundance were described by Coplen, 2011. Absolute values of 34S abundance are expressed as atom fraction 34S, x(34S) Eq. (1).where the total number of S atoms = 32S + 33S + 34S + 36S, whereas 34S enrichment (excess atom fraction 34S, xE (34S)sample/reference) is expressed by Eq. (2).
Relative 34S
Isotope-ratio analysis of S
The preparation of biological samples (e.g. soil, plant) for 34S/32S isotope-ratio analysis by mass spectrometry (IRMS) has been described in many publications (e.g. Krouse and Tabatabai, 1986, Hamilton et al., 1991, Krouse et al., 1996, Kester et al., 2001, Mayer and Krouse, 2004) and therefore will not be repeated here.
Sulfur isotope ratios are commonly measured as SO2 gas on the molecular ion masses 64 and 66. Unfortunately, the isotopes of oxygen directly interfere with the sulfur isotopes
Measurement parameters
Isotopic fractionation can occur as a result of physical (e.g. diffusion), chemical (equilibria or ion exchange) or biological (enzymatic i.e. kinetic) processes. It can be expressed by the fractionation factor (α) where α = in an equilibrium reaction, where s is a reactant (substrate) and p is a product. The fractionation factor is equivalent to the equilibrium constant (k) at a specified temperature. Isotopic fractionation can also be expressed as fractionation (Δ or ε) in values of per
Soils
There are few data on the distribution of δ34S in soils used for cropping and improved pastures, with most of the available data coming from natural ecosystems. The δ34S signatures of soils may differ between the different forms of S (organic vs. sulfate) and also may vary with soil depth (Table 2). Coplen et al., 2002a, Coplen et al., 2002b reported an extremely wide range of δ34S of soil organic S from −30 to +30‰. A much narrower range of δ34S of soil sulfate (+1.7 to +18.1‰) was reported
Efficiency of 34S-labelled fertilizers
S fertilizer efficiency can be estimated by the difference method, whereby the difference in the S uptake by a S fertilized and an unfertilized crop expressed as a fraction or percentage of the S fertilizer added is a measure of S fertilizer efficiency. This is an indirect method which assumes that the uptake of the soil sulfate is the same in both treatments. However, the indirect method may overestimate fertilizer use efficiency as the S fertilized plants are likely to have greater access to
Long-term agronomic experiments
Long-term experiments have been conducted in four European countries to determine the effect of mineral and organic fertilizer additions on the total S and 34S natural abundance in plant and soil samples (Table 7). Two of the studies conducted in the UK at Rothamsted focused on atmospheric S deposition by analysis of archived samples of grass herbage (Zhao et al., 1998) and wheat straw and grain (Zhao et al., 2003) from unfertilized plots spanning periods of 132 and 155 years, respectively (
S in plant physiological development
White clover (singly or mixed with grasses), wheat and canola plants grown in artificial media or soil in pots, tanks or bottles located in the glasshouse or growth room were labelled with 34SO42− to investigate the role of S in plant physiology, metabolism and ecology (Table 9). Plants were labelled at strategic times by addition of isotope to the growth medium or the plant foliage. The majority of studies were in solution culture and hydroponics (Table 9), and field studies have not been
Future opportunities for exploiting 34S to elucidate sulfur dynamics in agroecosystems
We have suggested four areas that in our opinion are worthy of further investigation using 34S as a tracer. Our assessment of future opportunities was based on observed movements in fertilizer technologies and usage, the global distribution of crops and climate change. There are also opportunities for the application of 34S in studies of animal physiology and the authentication of food (e.g. Inácio et al., 2015, Inácio and Chalk, 2017), although these topics were beyond the scope of the present
Conclusions
The objective of our review was to explore the role that 34S has played in tracing the dynamics of S in agro-ecosystems, and to identify future opportunities for exploiting 34S in applied agro-ecosystem research. A crucial question, however, concerns the usefulness of δ34S as a tracer compared with studies based on the use of 34S-enrichment or 34S-depletion. 34S natural abundance is an attractive approach because it does not perturb the system under study nor does it involve the purchase of
Acknowledgements
The senior author thanks the University of Melbourne for assistance with travel expenses, the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) for a visiting scientist fellowship (Pesquisador Visitante No 101.466/2014) and EMBRAPA-Solos as the host Institution. We thank Dr. S.K. Lam for preparing Fig. 2, Fig. 3.
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