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Assessment of soil quality using microbial properties and attributes of ecological relevance
Applied Soil Ecology 49 (2011) 1–4
Contents lists available at ScienceDirect
Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil
Viewpoint
Assessment of soil quality using microbial properties and attributes of ecological relevance Carlos Garbisu a , Itziar Alkorta b , Lur Epelde a,∗ a b
NEIKER-Tecnalia, Soil Microbial Ecology Group, Berreaga 1, E-48160 Derio, Spain Dept. Biochemistry and Molecular Biology, University of the Basque Country, UPV/EHU, E-48080 Bilbao, Spain
a r t i c l e
i n f o
Article history: Received 23 August 2010 Received in revised form 6 April 2011 Accepted 30 April 2011
Soil quality/soil health is frequently defined as “the capacity of soil to perform its functions” or “how well is the soil functioning for a specific goal or use” (Karlen et al., 2003). Although both terms are often used interchangeably, soil quality is generally associated with a soil’s fitness for a specific use whereas soil health is commonly used in a broader sense to indicate the capacity of soil to function as a vital living system to sustain biological productivity, promote environmental quality, and maintain plant and animal health (Doran and Zeiss, 2000). In any case, the difference between both terms is not within the scope of this paper (the term soil quality will then be used throughout this paper). The term “functions” has teleological and anthropocentric connotations, but it has proven to be easily understood by many non-scientists, most notably, decision makers. Although debatable and imperfect (Sojka and Upchurch, 1999; Sojka et al., 2003), the concept of soil quality (Doran and Parkin, 1994, 1996; Karlen et al., 2001) has helped attract much needed attention towards the conservation of soil as a most valuable resource. In the last years, the ecosystem services approach (ecosystem services are the multiple benefits provided by ecosystems to humans) has been adopted by many of those involved in the conservation of ecosystems, biodiversity, etc. Consequently, some authors (Velasquez et al., 2007) proposed an indicator of soil quality (GISQ) that evaluates soil ecosystem services, assuming that “the more ecosystem services produced, the better soil quality”. Though the concept of ecosystem services is by definition human-centered, the GISQ appears an interesting approach as a multifunctional indicator of soil quality. It is a well-known fact that soil physical and chemical characteristics, as well as non-microbial soil organisms, can be used as indicators of soil quality. Likewise, soil microbial properties (which,
∗ Corresponding author. E-mail address: [email protected] (L. Epelde). 0929-1393/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.apsoil.2011.04.018
on the other hand, are frequently statistically correlated with soil physical and chemical parameters) are being increasingly used as indicators of soil quality owing to their rapid response, sensitivity and capacity to provide information that integrates many environmental factors (Mijangos et al., 2006). Soil microbial properties have been reported to be effective and consistent indicators of management induced changes to soil quality (Bending et al., 2004). After all, microbial communities play a key role in many soil processes and the delivery of essential ecosystem services (Jeffery et al., 2010), i.e., they can provide a direct measure of soil functioning. Numerous reviews have been published on the utilization of microbial properties as indicators of soil quality (Bloem et al., 2006; Ritz et al., 2009; Schloter et al., 2003). Some commonly used microbial indicators are: (i) biomass indicators: microbial biomass C, substrate-induced respiration, ATP content; (ii) activity indicators: basal respiration, mineralizable N, nitrification rate, enzyme activities; and (iii) diversity indicators: community-level physiological and genetic profiles. The soil quality concept has focused increased interest on integrating soil microbiological assessments into soil evaluation (Kennedy and Papendick, 1995; Sojka and Upchurch, 1999). While discussing their reservations regarding the soil quality concept, Sojka and Upchurch (1999) expressed their concern on the fact that the roles and functions of soil microorganisms are yet to be fully explained. In this context, many of us (Epelde et al., 2009; Hernández-Allica et al., 2006; Mijangos et al., 2006) have been inferring the impact of disturbances on soil quality directly from the values of soil microbial properties. Nevertheless, while doing so, we frequently “feel” that there is still an unsolved gap between our specific measurements and the concept of soil quality. After all, microbial measurements are frequently highly context-dependent (they depend, among other factors, on the geographic area, specific location, climate, soil type, soil history, etc.). Therefore, we need to search for more general indicators that are less context-dependent (i.e., more “universal”). In this respect, biodiversity, stability and self-recovery from stress have been suggested as universal
2
C. Garbisu et al. / Applied Soil Ecology 49 (2011) 1–4
indicators of soil quality (Parr et al., 1992; van Bruggen and Semenov, 2000). Following the same line of thought, we propose that, for a better interpretation of soil microbial properties as indicators of soil quality, it can also be very helpful to link the concept of soil quality to that of ecosystem function (i.e., ecosystem health, sensu Rapport, 1998) through the grouping of soil microbial properties within a set of ecosystem attributes of ecological relevance. Here, it is noteworthy to remember that the use of the health metaphor at the ecosystem level, although most powerful as a communication device, is based on analogy rather than homology (ecosystems are not organisms!) (Rapport, 1998). Similarly, van Bruggen and Semenov (2000) indicated that soil quality could be considered a subset of ecosystem function. The concept of ecosystem function (i.e., ecosystem health) was elaborated as a measure of system’s (i) vigor, which may be operationally quantified in terms of productivity, or throughput of material or energy in the system. Indeed, the vigor of a system is a measure of its activity, metabolism, or primary productivity; (ii) organization, which may be assessed in terms of both the diversity of components and their degree of mutual dependence, that is, by studying the exchange pathways between them. Measures of organization are affected by both the diversity of species and the number of pathways of material exchange between each component. A greater diversity of organisms offers a priori a greater potential for interactions; and (iii) stability, which may be determined in terms of the system’s ability to maintain its structure and pattern of behaviour in the presence of stress (Rapport, 1998). Relevantly, van Bruggen and Semenov (2000) proposed that the responses of a soil sample to different stresses can be better indicators of soil quality than soil characteristics measured without imposing stress. These authors suggested to subject soil samples to several stresses and monitor microbial responses at regular intervals after application of stress. On the other hand, a properly functioning ecosystem must be characterized by integrity of nutrient cycles and energy flows, and cannot be harmful to surrounding ecosystems. Another attribute most useful for the assessment of soil quality is suppressiveness: suppressive soils are soils in which disease severity or incidence remains low, despite the presence of a pathogen, a susceptible host plant, and climatic conditions favourable for disease development (Janvier et al., 2007; van Bruggen and Semenov, 2000). Plant disease suppression by itself cannot be equated with soil quality (Hornby and Bateman, 1997) but it can be an essential function of a good quality soil (van Bruggen and Semenov, 2000). Interestingly, it has been suggested (van Bruggen and Semenov, 2000) that indicators of soil quality could possibly also function as indicators of disease suppressiveness (soil respiration, enzyme activities, N mineralization, the ratio of oligotrophs to copiotrophs, etc. have been associated with a reduction in disease incidence) (Janvier et al., 2007). In addition, redundancy can be a most relevant attribute when assessing soil quality, as functions may not be affected by the loss of a species from an ecosystem if other species are able to perform the same function (Jeffery et al., 2010). According to the ‘redundant species’ hypothesis, only a minimum number of species is needed for ecosystems to function (Naeem et al., 1995) and the loss of a functionally redundant species would have very little impact, or none at all, on the ecosystem services provided (Naeem et al., 1995; Hunt and Wall, 2002). By contrast, other authors (Wolters, 2001) consider that the fact that soil species appear functionally ‘redundant’ is rather related to our lack of understanding of the functioning of the soil ecosystem. Redundancy can be highly context-dependent since spatial and temporal environmental variability may provide room for functional redundancy at small spatial and temporal scales, but is not expected to do so at the larger
scales at which environmental variations help maintain coexistence (Loreau, 2004). The five attributes (vigor, organization, stability, suppressiveness, redundancy) presented here overlap with each other to a certain extent, but are at the same time complementary (that is why, when possible, all five attributes should be measured when assessing soil quality). For instance, although the relationship between microbial structural diversity and soil function is still largely unknown (Torsvik and Øvreås, 2002), structural biodiversity (organization) is most likely to influence vigor, stability, suppressiveness and redundancy. As abovementioned, a greater biodiversity offers a greater potential for interactions, and a more complex network of interactions is normally more adaptive to change and resilient to disturbance. Similarly, the more organisms there are that can perform a specific soil function, the more likely it is that if some are removed the function will remain unaffected (higher levels of redundancy). Likewise, Moore et al. (1993) found that the time needed for a soil to return to steady state after perturbation declined exponentially with an increase in primary productivity (vigor), which in soil is determined by the return of plant-derived organic matter to the soil. From all of the above, a new definition of soil quality is proposed: “Soil quality is the capacity of a given soil to sustainably perform its ecological processes, functions and ecosystem services, and maintain a suite of essential ecosystem attributes of ecological relevance (vigor, organization, stability, suppressiveness, redundancy) at a level similar to that of a reference soil, without causing an adverse impact on the proper functioning of surrounding ecosystems or human health”. A shorter, more operative definition would be: “Soil quality is the capacity of a soil to perform its ecosystem processes and services, while maintaining ecosystem attributes of ecological relevance”. When assessing the impact of a disturbance on soil quality, one can state how it affects each of these attributes with respect to a reference soil. Alternatively, Karlen et al. (2001) claim that trends and changes over time provide the only feasible way to project the effects of soil management or land use on the sustainability of a natural resource that is dynamic, living and ever changing such as soil. Regarding soil quality trends over time, the assumption that “the higher the value of the ecosystem attribute, the better soil quality” appears valid for most situations (i.e., end uses): the higher organization the better, the higher stability the better, the higher suppressiveness the better, and the higher redundancy the better. Regarding vigor, depending on the specific soil use and function, this assumption might not be true and, accordingly, if the different attributes are pondered (see below), vigor should probably have a lower weight. After all, vigor refers to a throughput of energy that can be measured in terms of nutrient cycling and productivity, and in some cases it is not true that the higher the throughput the better (Rapport, 1998). Nonetheless, it has been hypothesized that, at least for most ecosystems, more stress is associated with less vigor in terms of productivity and throughput (Rapport, 1998). Most importantly, soil quality has to be assessed based on what use the soil is intended for: a soil that has an excellent quality for one purpose can have very poor quality for another. Certainly, reasons for assessing soil quality in an agricultural system may be different than in a natural ecosystem: in an agricultural system, soil quality may be managed to maximize yield without negative environmental impact, while in a natural ecosystem, soil quality may be observed as a baseline value or set of values against which future changes in the system may be compared (Singer and Ewing, 2000). However, within the context of “soil quality for use”, we must take into consideration the current lack of understanding regarding the openness and interconnectedness of ecosystems on scales that transcend management boundaries (Karlen et al., 2001).
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CONVENTIONAL APPROACH Enzyme activities Soil respiration Microbial biomass carbon Community-level profiles Nitrification potential rate Etc.
3
ALTERNATIVE APPROACH Enzyme activities Soil respiration Microbial biomass carbon Community-level profiles Nitrification potential rate Etc.
Vigor Organization Stability Suppressiveness Redundancy
Soil quality
Soil quality
Fig. 1. Assessment of soil quality: conventional approach versus alternative approach. The alternative approach includes the grouping of microbial indicators of soil quality within ecosystem attributes of ecological relevance.
Also, for each soil use, we must identify critical functions (depending on the soil use, some functions will be more important than others) and select appropriate indicators for each of them (an example of the linkage between soil functions and indicators is shown in Karlen et al., 2001). But, as abovementioned, in general, the higher the value of the ecosystem attribute the better soil quality for all soil uses. When two soils perform a specific function at a similar level, the one presenting higher values of the ecologically relevant attributes might be considered of a higher quality. Finally, for valid comparison of soil quality across variations in climate, soil and management, reference guidelines and thresholds for soil quality indicators are needed, taken into consideration appropriate scales of time and space for soil quality assessment (Doran and Parkin, 1994; Karlen et al., 2001). A major research effort is still needed to calibrate soil quality indicators that allows interpretation, independent of soil type. Regarding the assignment of microbial properties within each attribute, as an example, we tentatively propose that: (i) vigor can be measured from microbial biomass C, respiration, overall enzyme activity, ATP content, plant productivity, etc.; (ii) organization can be determined from microbial biodiversity indicators (e.g., community-level genetic profiles with PCR-DGGE, phospholipid fatty acid profiles, phylogenetic microarrays, metagenome sequencing) and measurements of the status of microbial-based soil food webs (e.g., trophic-level biomasses, nucleic acid-based stable isotope probing, phospholipid fatty acid-based stable isotope probing); (iii) stability can be assessed through the integration of resistance and resilience indexes (Griffiths et al., 2000) calculated, after the application of a variety of stresses and levels of stress intensity, by means of studying their effect on, for instance, basal respiration, N mineralization, nitrification rate, etc.; (iv) suppressiveness can be evaluated through suppression of mycelial growth for fungistasis (the suppressiveness of soils to the germination and growth of fungi), bioassays for plant disease incidence against different pathogens, etc.; and (v) redundancy can be determined according to the number of species present within specific functional groups (nitrifiers, denitrifiers, chitin-degraders, etc.) through PCR-DGGE, or through redundancy of functional genes via microarray analysis. As the order of magnitude of the analytical results of the different soil microbial properties varies considerably, to avoid some properties having more weight than others during the calculation of the corresponding attribute, values can be normalized to, for
example, 100% (100% = value obtained for each specific microbial parameter in the reference soil). There still remains the question of the weighting of the different microbial properties within each attribute, which must be done according to a set of chosen criteria (an interesting discussion on scaling and weighting can be found in Jensen and Mesman, 2006; in any case, the use of the weighted geometric mean is recommended). Likewise, if one needs an integrated value of soil quality, the different attributes must also be pondered again. Fig. 1 graphically represents this approach to the assessment of soil quality. Most of these concepts have traditionally been used by many soil scientists, using the same or different names. Our intention is not to rename old concepts here but simply to highlight a most frequently forgotten aspect, i.e., the usefulness of focusing our interpretations towards ecosystem attributes of ecological relevance when assessing soil quality. And, of course, we do not claim to have the final answer to the many difficulties associated with soil quality assessment (Sojka and Upchurch, 1999; Karlen et al., 2001). The objective of this paper is simply to do our part (hopefully, a little step forward) in this field by means of emphasizing that the concept of soil quality can be linked to that of ecosystem function through the grouping of microbial properties within a set of ecosystem attributes of ecological relevance. As occurs with the use of indices, this approach results in information compression and can lead to an oversimplification of available information. Therefore, it might be a good idea to assess soil quality at two different levels, the indicator level and the attribute level, since they provide complementary information. Moreover, when interpreting data on soil quality, soil managers, decision makers and alike will probably feel more comfortable with terms such as vigor, organization, stability, redundancy, etc., than with terms such as microbial biomass C, arylsulfatase activity, substrate-induced respiration, ATP content, etc. We do hope this approach can help reduce the gap between measurements of soil microbial properties and the concept of soil quality, as well as facilitate the communication between scientists and non-scientist stakeholders. Acknowledgements The authors sincerely thank the Editor and Reviewers for their helpful comments which have considerably improved the manuscript. This work has been financially supported by
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the Spanish Ministry of Science and Innovation (PAISAIA-3 project, CGL2005-08046-C03-02/BOS) and the Basque Government (BERRILUR-3 project). References Bending, G.D., Turner, M.K., Rayns, F., Marx, M.C., Wood, M., 2004. Microbial and biochemical soil quality indicators and their potential for differentiating areas under contrasting agricultural management regimes. Soil Biol. Biochem. 36, 1785–1792. Bloem, J., Hopkins, D., Benedetti, A., 2006. Microbiological Methods for Assessing Soil Quality. CABI Publishing, Wallingford. Doran, J.W., Parkin, T.B., 1994. Defining and assessing soil quality. In: Doran, J.W., Coleman, D.C., Bezdicek, D.F., Stewart, B.A. (Eds.), Defining Soil Quality for a Sustainable Environment. Soil Science Society of America, Madison, pp. 3–21. Doran, J.W., Parkin, T.B., 1996. Quantitative indicators of soil quality: a minimum data set. In: Methods for Assessing Soil Quality. SSSA, pp. 25–37 (Special publication no. 49). Doran, J.W., Zeiss, M.R., 2000. Soil health and sustainability: managing the biotic component of soil quality. Appl. Soil Ecol. 15, 3–11. Epelde, L., Mijangos, I., Becerril, J.M., Garbisu, C., 2009. Soil microbial community as bioindicator of the recovery of soil functioning derived from metal phytoextraction with sorghum. Soil Biol. Biochem. 41, 1788–1794. Griffiths, B.S., Ritz, K., Bardgett, R.D., Cook, R., Christensen, S., Ekelund, F., Sorensen, S.J., Bååth, E., Bloem, J., Ruiter, P.C., Dolfing, J., Nicolardot, B., 2000. Ecosystem response of pasture soil communities to fumigation-induced microbial diversity reductions: an examination of the biodiversity–ecosystem function relationship. Oikos 90, 279–294. Hernández-Allica, J., Becerril, J.M., Zárate, O., Garbisu, C., 2006. Assessment of the efficiency of a metal phytoextraction process with biological indicators of soil health. Plant Soil 281, 147–158. Hornby, D., Bateman, G.L., 1997. Potential use of plant root pathogens as bioindicators of soil health. In: Pankhurst, C., Doube, B.M., Gupta, V.V.S.R. (Eds.), Biological Indicators of Soil Health. CAB Int., Wallingford, pp. 179–200. Hunt, H.W., Wall, D.H., 2002. Modelling the effects of loss of soil biodiversity on ecosystem function. Global Change Biol. 8, 33–50. Janvier, C., Villeneuve, F., Alabouvette, C., Edel-Hermann, V., Mateille, T., Steinberg, C., 2007. Soil health through soil disease suppression: which strategy from descriptors to indicators? Soil Biol. Biochem. 39, 1–23. Jeffery, S., Gardi, C., Jones, A., Montanarella, L., Marmo, L., Miko, L., Ritz, K., Peres, G., Römbke, J., van der Putten, W.H., 2010. European Atlas of Soil Biodiversity. European Commission. Publications Office of the European Union, Luxembourg.
Jensen, J., Mesman, M., 2006. Ecological Risk Assessment of Contaminated Land. Decision Support for Site-specific Investigations. RIVM, Bilthoven, The Netherlands. Karlen, D.L., Andrews, S.S., Doran, J.W., 2001. Soil quality: current concepts and applications. In: Sparks, D.L. (Ed.), Advances in Agronomy, vol. 74. Academic Press, New York, pp. 1–40. Karlen, D.L., Andrews, S.S., Weinhold, B.J., Doran, J.W., 2003. Soil quality: humankind’s foundation for survival. J. Soil Water Conserv. 58, 171–179. Kennedy, A.C., Papendick, R.I., 1995. Microbial characteristics of soil quality. J. Soil Water Conserv. 50, 243–248. Loreau, L., 2004. Does functional redundancy exist? OIKOS 104, 606–611. Mijangos, I., Pérez, R., Albizu, I., Garbisu, C., 2006. Effects of fertilization and tillage on soil biological parameters. Enzym. Microb. Technol. 40, 100–106. Moore, J.C., de Ruiter, P.C., Hunt, H.W., 1993. Influence of productivity on the stability of real and model ecosystems. Science 261, 906–908. Naeem, S., Thompson, L.J., Lawler, S.P., Lawton, J.H., Woodfin, R.M., 1995. Empiricalevidence that declining species-diversity may alter the performance of terrestrial ecosystems. Philos. Trans. Roy. Soc. Lond. Ser. B: Biol. Sci. 347, 249–262. Parr, J.F., Papendick, R.I., Hornick, S.B., Meyer, R.E., 1992. Soil quality: attributes and relationship to alternative and sustainable agriculture. Am. J. Altern. Agric. 7, 5–11. Rapport, D., 1998. Defining ecosystem health. In: Rapport, D., Costanza, R., Epstein, P.R., Gaudet, C., Levins, R. (Eds.), Ecosystem Health. Blackwell Science, Oxford, pp. 18–33. Ritz, K., Black, H.I.J., Campbell, C.D., Harris, J.A., Wood, C., 2009. Selecting biological indicators for monitoring soils: a framework for balancing scientific and technical opinion to assist policy development. Ecol. Indic. 9, 1212–1221. Schloter, M., Dilly, O., Munch, J.C., 2003. Indicators for evaluating soil quality. Agric. Ecosyst. Environ. 98, 255–262. Singer, M.J., Ewing, S., 2000. Soil quality. In: Sumner, M.E. (Ed.), Handbook of Soil Science. CRC Press, Boca Raton, pp. G271–G298. Sojka, R.E., Upchurch, D.R., 1999. Reservations regarding the soil quality concept. Soil Sci. Soc. Am. J. 63, 1039–1054. Sojka, R.E., Upchurch, D.R., Borlaug, N.E., 2003. Quality soil management or soil quality management: performance versus semantics. In: Sparks, D.L. (Ed.), Advances in Agronomy, vol. 79. Academic Press, New York, pp. 1–68. Torsvik, V., Øvreås, L., 2002. Microbial diversity and function in soil: from genes to ecosystems. Curr. Opin. Microbiol. 5, 240–245. van Bruggen, A.H.C., Semenov, A.M., 2000. In search of biological indicators for soil health and disease suppression. Appl. Soil Ecol. 15, 13–24. Velasquez, E., Lavelle, P., Andrade, M., 2007. GISQ, a multifunctional indicator of soil quality. Soil Biol. Biochem. 39, 3066–3080. Wolters, V., 2001. Biodiversity of soil animals and its function. Eur. J. Soil Biol. 37, 221–227.
Contents lists available at ScienceDirect
Applied Soil Ecology journal homepage: www.elsevier.com/locate/apsoil
Viewpoint
Assessment of soil quality using microbial properties and attributes of ecological relevance Carlos Garbisu a , Itziar Alkorta b , Lur Epelde a,∗ a b
NEIKER-Tecnalia, Soil Microbial Ecology Group, Berreaga 1, E-48160 Derio, Spain Dept. Biochemistry and Molecular Biology, University of the Basque Country, UPV/EHU, E-48080 Bilbao, Spain
a r t i c l e
i n f o
Article history: Received 23 August 2010 Received in revised form 6 April 2011 Accepted 30 April 2011
Soil quality/soil health is frequently defined as “the capacity of soil to perform its functions” or “how well is the soil functioning for a specific goal or use” (Karlen et al., 2003). Although both terms are often used interchangeably, soil quality is generally associated with a soil’s fitness for a specific use whereas soil health is commonly used in a broader sense to indicate the capacity of soil to function as a vital living system to sustain biological productivity, promote environmental quality, and maintain plant and animal health (Doran and Zeiss, 2000). In any case, the difference between both terms is not within the scope of this paper (the term soil quality will then be used throughout this paper). The term “functions” has teleological and anthropocentric connotations, but it has proven to be easily understood by many non-scientists, most notably, decision makers. Although debatable and imperfect (Sojka and Upchurch, 1999; Sojka et al., 2003), the concept of soil quality (Doran and Parkin, 1994, 1996; Karlen et al., 2001) has helped attract much needed attention towards the conservation of soil as a most valuable resource. In the last years, the ecosystem services approach (ecosystem services are the multiple benefits provided by ecosystems to humans) has been adopted by many of those involved in the conservation of ecosystems, biodiversity, etc. Consequently, some authors (Velasquez et al., 2007) proposed an indicator of soil quality (GISQ) that evaluates soil ecosystem services, assuming that “the more ecosystem services produced, the better soil quality”. Though the concept of ecosystem services is by definition human-centered, the GISQ appears an interesting approach as a multifunctional indicator of soil quality. It is a well-known fact that soil physical and chemical characteristics, as well as non-microbial soil organisms, can be used as indicators of soil quality. Likewise, soil microbial properties (which,
∗ Corresponding author. E-mail address: [email protected] (L. Epelde). 0929-1393/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.apsoil.2011.04.018
on the other hand, are frequently statistically correlated with soil physical and chemical parameters) are being increasingly used as indicators of soil quality owing to their rapid response, sensitivity and capacity to provide information that integrates many environmental factors (Mijangos et al., 2006). Soil microbial properties have been reported to be effective and consistent indicators of management induced changes to soil quality (Bending et al., 2004). After all, microbial communities play a key role in many soil processes and the delivery of essential ecosystem services (Jeffery et al., 2010), i.e., they can provide a direct measure of soil functioning. Numerous reviews have been published on the utilization of microbial properties as indicators of soil quality (Bloem et al., 2006; Ritz et al., 2009; Schloter et al., 2003). Some commonly used microbial indicators are: (i) biomass indicators: microbial biomass C, substrate-induced respiration, ATP content; (ii) activity indicators: basal respiration, mineralizable N, nitrification rate, enzyme activities; and (iii) diversity indicators: community-level physiological and genetic profiles. The soil quality concept has focused increased interest on integrating soil microbiological assessments into soil evaluation (Kennedy and Papendick, 1995; Sojka and Upchurch, 1999). While discussing their reservations regarding the soil quality concept, Sojka and Upchurch (1999) expressed their concern on the fact that the roles and functions of soil microorganisms are yet to be fully explained. In this context, many of us (Epelde et al., 2009; Hernández-Allica et al., 2006; Mijangos et al., 2006) have been inferring the impact of disturbances on soil quality directly from the values of soil microbial properties. Nevertheless, while doing so, we frequently “feel” that there is still an unsolved gap between our specific measurements and the concept of soil quality. After all, microbial measurements are frequently highly context-dependent (they depend, among other factors, on the geographic area, specific location, climate, soil type, soil history, etc.). Therefore, we need to search for more general indicators that are less context-dependent (i.e., more “universal”). In this respect, biodiversity, stability and self-recovery from stress have been suggested as universal
2
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indicators of soil quality (Parr et al., 1992; van Bruggen and Semenov, 2000). Following the same line of thought, we propose that, for a better interpretation of soil microbial properties as indicators of soil quality, it can also be very helpful to link the concept of soil quality to that of ecosystem function (i.e., ecosystem health, sensu Rapport, 1998) through the grouping of soil microbial properties within a set of ecosystem attributes of ecological relevance. Here, it is noteworthy to remember that the use of the health metaphor at the ecosystem level, although most powerful as a communication device, is based on analogy rather than homology (ecosystems are not organisms!) (Rapport, 1998). Similarly, van Bruggen and Semenov (2000) indicated that soil quality could be considered a subset of ecosystem function. The concept of ecosystem function (i.e., ecosystem health) was elaborated as a measure of system’s (i) vigor, which may be operationally quantified in terms of productivity, or throughput of material or energy in the system. Indeed, the vigor of a system is a measure of its activity, metabolism, or primary productivity; (ii) organization, which may be assessed in terms of both the diversity of components and their degree of mutual dependence, that is, by studying the exchange pathways between them. Measures of organization are affected by both the diversity of species and the number of pathways of material exchange between each component. A greater diversity of organisms offers a priori a greater potential for interactions; and (iii) stability, which may be determined in terms of the system’s ability to maintain its structure and pattern of behaviour in the presence of stress (Rapport, 1998). Relevantly, van Bruggen and Semenov (2000) proposed that the responses of a soil sample to different stresses can be better indicators of soil quality than soil characteristics measured without imposing stress. These authors suggested to subject soil samples to several stresses and monitor microbial responses at regular intervals after application of stress. On the other hand, a properly functioning ecosystem must be characterized by integrity of nutrient cycles and energy flows, and cannot be harmful to surrounding ecosystems. Another attribute most useful for the assessment of soil quality is suppressiveness: suppressive soils are soils in which disease severity or incidence remains low, despite the presence of a pathogen, a susceptible host plant, and climatic conditions favourable for disease development (Janvier et al., 2007; van Bruggen and Semenov, 2000). Plant disease suppression by itself cannot be equated with soil quality (Hornby and Bateman, 1997) but it can be an essential function of a good quality soil (van Bruggen and Semenov, 2000). Interestingly, it has been suggested (van Bruggen and Semenov, 2000) that indicators of soil quality could possibly also function as indicators of disease suppressiveness (soil respiration, enzyme activities, N mineralization, the ratio of oligotrophs to copiotrophs, etc. have been associated with a reduction in disease incidence) (Janvier et al., 2007). In addition, redundancy can be a most relevant attribute when assessing soil quality, as functions may not be affected by the loss of a species from an ecosystem if other species are able to perform the same function (Jeffery et al., 2010). According to the ‘redundant species’ hypothesis, only a minimum number of species is needed for ecosystems to function (Naeem et al., 1995) and the loss of a functionally redundant species would have very little impact, or none at all, on the ecosystem services provided (Naeem et al., 1995; Hunt and Wall, 2002). By contrast, other authors (Wolters, 2001) consider that the fact that soil species appear functionally ‘redundant’ is rather related to our lack of understanding of the functioning of the soil ecosystem. Redundancy can be highly context-dependent since spatial and temporal environmental variability may provide room for functional redundancy at small spatial and temporal scales, but is not expected to do so at the larger
scales at which environmental variations help maintain coexistence (Loreau, 2004). The five attributes (vigor, organization, stability, suppressiveness, redundancy) presented here overlap with each other to a certain extent, but are at the same time complementary (that is why, when possible, all five attributes should be measured when assessing soil quality). For instance, although the relationship between microbial structural diversity and soil function is still largely unknown (Torsvik and Øvreås, 2002), structural biodiversity (organization) is most likely to influence vigor, stability, suppressiveness and redundancy. As abovementioned, a greater biodiversity offers a greater potential for interactions, and a more complex network of interactions is normally more adaptive to change and resilient to disturbance. Similarly, the more organisms there are that can perform a specific soil function, the more likely it is that if some are removed the function will remain unaffected (higher levels of redundancy). Likewise, Moore et al. (1993) found that the time needed for a soil to return to steady state after perturbation declined exponentially with an increase in primary productivity (vigor), which in soil is determined by the return of plant-derived organic matter to the soil. From all of the above, a new definition of soil quality is proposed: “Soil quality is the capacity of a given soil to sustainably perform its ecological processes, functions and ecosystem services, and maintain a suite of essential ecosystem attributes of ecological relevance (vigor, organization, stability, suppressiveness, redundancy) at a level similar to that of a reference soil, without causing an adverse impact on the proper functioning of surrounding ecosystems or human health”. A shorter, more operative definition would be: “Soil quality is the capacity of a soil to perform its ecosystem processes and services, while maintaining ecosystem attributes of ecological relevance”. When assessing the impact of a disturbance on soil quality, one can state how it affects each of these attributes with respect to a reference soil. Alternatively, Karlen et al. (2001) claim that trends and changes over time provide the only feasible way to project the effects of soil management or land use on the sustainability of a natural resource that is dynamic, living and ever changing such as soil. Regarding soil quality trends over time, the assumption that “the higher the value of the ecosystem attribute, the better soil quality” appears valid for most situations (i.e., end uses): the higher organization the better, the higher stability the better, the higher suppressiveness the better, and the higher redundancy the better. Regarding vigor, depending on the specific soil use and function, this assumption might not be true and, accordingly, if the different attributes are pondered (see below), vigor should probably have a lower weight. After all, vigor refers to a throughput of energy that can be measured in terms of nutrient cycling and productivity, and in some cases it is not true that the higher the throughput the better (Rapport, 1998). Nonetheless, it has been hypothesized that, at least for most ecosystems, more stress is associated with less vigor in terms of productivity and throughput (Rapport, 1998). Most importantly, soil quality has to be assessed based on what use the soil is intended for: a soil that has an excellent quality for one purpose can have very poor quality for another. Certainly, reasons for assessing soil quality in an agricultural system may be different than in a natural ecosystem: in an agricultural system, soil quality may be managed to maximize yield without negative environmental impact, while in a natural ecosystem, soil quality may be observed as a baseline value or set of values against which future changes in the system may be compared (Singer and Ewing, 2000). However, within the context of “soil quality for use”, we must take into consideration the current lack of understanding regarding the openness and interconnectedness of ecosystems on scales that transcend management boundaries (Karlen et al., 2001).
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CONVENTIONAL APPROACH Enzyme activities Soil respiration Microbial biomass carbon Community-level profiles Nitrification potential rate Etc.
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ALTERNATIVE APPROACH Enzyme activities Soil respiration Microbial biomass carbon Community-level profiles Nitrification potential rate Etc.
Vigor Organization Stability Suppressiveness Redundancy
Soil quality
Soil quality
Fig. 1. Assessment of soil quality: conventional approach versus alternative approach. The alternative approach includes the grouping of microbial indicators of soil quality within ecosystem attributes of ecological relevance.
Also, for each soil use, we must identify critical functions (depending on the soil use, some functions will be more important than others) and select appropriate indicators for each of them (an example of the linkage between soil functions and indicators is shown in Karlen et al., 2001). But, as abovementioned, in general, the higher the value of the ecosystem attribute the better soil quality for all soil uses. When two soils perform a specific function at a similar level, the one presenting higher values of the ecologically relevant attributes might be considered of a higher quality. Finally, for valid comparison of soil quality across variations in climate, soil and management, reference guidelines and thresholds for soil quality indicators are needed, taken into consideration appropriate scales of time and space for soil quality assessment (Doran and Parkin, 1994; Karlen et al., 2001). A major research effort is still needed to calibrate soil quality indicators that allows interpretation, independent of soil type. Regarding the assignment of microbial properties within each attribute, as an example, we tentatively propose that: (i) vigor can be measured from microbial biomass C, respiration, overall enzyme activity, ATP content, plant productivity, etc.; (ii) organization can be determined from microbial biodiversity indicators (e.g., community-level genetic profiles with PCR-DGGE, phospholipid fatty acid profiles, phylogenetic microarrays, metagenome sequencing) and measurements of the status of microbial-based soil food webs (e.g., trophic-level biomasses, nucleic acid-based stable isotope probing, phospholipid fatty acid-based stable isotope probing); (iii) stability can be assessed through the integration of resistance and resilience indexes (Griffiths et al., 2000) calculated, after the application of a variety of stresses and levels of stress intensity, by means of studying their effect on, for instance, basal respiration, N mineralization, nitrification rate, etc.; (iv) suppressiveness can be evaluated through suppression of mycelial growth for fungistasis (the suppressiveness of soils to the germination and growth of fungi), bioassays for plant disease incidence against different pathogens, etc.; and (v) redundancy can be determined according to the number of species present within specific functional groups (nitrifiers, denitrifiers, chitin-degraders, etc.) through PCR-DGGE, or through redundancy of functional genes via microarray analysis. As the order of magnitude of the analytical results of the different soil microbial properties varies considerably, to avoid some properties having more weight than others during the calculation of the corresponding attribute, values can be normalized to, for
example, 100% (100% = value obtained for each specific microbial parameter in the reference soil). There still remains the question of the weighting of the different microbial properties within each attribute, which must be done according to a set of chosen criteria (an interesting discussion on scaling and weighting can be found in Jensen and Mesman, 2006; in any case, the use of the weighted geometric mean is recommended). Likewise, if one needs an integrated value of soil quality, the different attributes must also be pondered again. Fig. 1 graphically represents this approach to the assessment of soil quality. Most of these concepts have traditionally been used by many soil scientists, using the same or different names. Our intention is not to rename old concepts here but simply to highlight a most frequently forgotten aspect, i.e., the usefulness of focusing our interpretations towards ecosystem attributes of ecological relevance when assessing soil quality. And, of course, we do not claim to have the final answer to the many difficulties associated with soil quality assessment (Sojka and Upchurch, 1999; Karlen et al., 2001). The objective of this paper is simply to do our part (hopefully, a little step forward) in this field by means of emphasizing that the concept of soil quality can be linked to that of ecosystem function through the grouping of microbial properties within a set of ecosystem attributes of ecological relevance. As occurs with the use of indices, this approach results in information compression and can lead to an oversimplification of available information. Therefore, it might be a good idea to assess soil quality at two different levels, the indicator level and the attribute level, since they provide complementary information. Moreover, when interpreting data on soil quality, soil managers, decision makers and alike will probably feel more comfortable with terms such as vigor, organization, stability, redundancy, etc., than with terms such as microbial biomass C, arylsulfatase activity, substrate-induced respiration, ATP content, etc. We do hope this approach can help reduce the gap between measurements of soil microbial properties and the concept of soil quality, as well as facilitate the communication between scientists and non-scientist stakeholders. Acknowledgements The authors sincerely thank the Editor and Reviewers for their helpful comments which have considerably improved the manuscript. This work has been financially supported by
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