Romul_Hum model of soil organic matter formation coupled with soil biota activity. III. Parameterisation of earthworm activity
Introduction
Modelling the dynamics of soil organic matter (SOM) is critical to proper representation of the soil system and its role in ecosystems (Benbi and Richter, 2002, Manzoni and Porporato, 2009, Larocque et al., 2016). Through biotic and abiotic processes SOM is formed in, and lost from (primarily as carbon-dioxide), the soil system. However, models used for ecosystem, landscape, regional and global assessment of carbon (C) rarely include processes and agents active in SOM formation. Rather, they focus on loss of soil C because of the great interest in the contribution of soil C to greenhouse gasses (i.e., carbon-dioxide) (Komarov et al., 2007, Huang et al., 2010, Braakhekke et al., 2011). In addition most soil C models do not account for the role of soil fauna in C dynamics (formation and loss) (Smith et al., 1997, Smith et al., 1998, Manzoni and Porporato, 2009). Earthworms are soil fauna that are well known to play a significant role in soil development through their effects on SOM (Edwards and Bohlen, 1996, Lavelle, 1997, Bouché, 2014, De Wandeler et al., 2016). One reason SOM models have not made significant advances in recent decades is the failure to include key agents and processes that are well known to affect SOM dynamics (Schmidt et al., 2011) and this includes earthworms acting as agents of soil organic matter formation.
The soil-forming activities of earthworms were appreciated as far back as the late19th century (Darwin, 1881; Müller, 1887) and are acknowledged in the modern scientific literature (Ekschmitt et al., 2008, Edwards et al., 2013). The importance of soil biota to SOM formation is embedded in the concepts of humus forms and their development (Kubiëna, 1953, Chertov, 1981, Baritz, 2003, Galvan et al., 2006, Blouin et al., 2013; Chertov and Komarov, 2013). Earthworms play a critical role in the formation of the mull humus form (Zanella et al., 2011, Ponge et al., 2014) which is characterized by the presence of highly transformed organic matter (OM) that is intimately associated with inorganic soil components. Experimental data has shown that earthworms form recalcitrant SOM in silt and clay fractions (Shaw and Pawluk, 1986, Fox et al., 2006), and that humic substances are actively formed and modified in earthworms casts (Frouz et al., 2011, Tikhonov et al., 2011) or microaggregates within casts (Bossuyt et al., 2005). Thus casts and the “drilosphere” (Schrader et al., 2007) are recognized as zones of SOM sequestration (Frouz et al., 2011, Blouin et al., 2013). The role of earthworms in SOM accumulation and protection is now considered an adaptation mechanism for stabilisation of animal habitat (Wolters, 2000).
Earthworms are the most commonly and easily recognized representative of soil macrofauna that are responsible both for physical and biochemical transformation of organic debris (Edwards and Bohlen, 1996, Lavelle, 1997). They are divided into three morpho-ecological groups (Edwards and Bohlen, 1996): epigeic earthworms, which inhabit organic soil layers; anecic earthworms, which inhabit permanent burrows, consume mostly leaf litter and transfer it to the mineral topsoil; and endogeic earthworms, which inhabit the mineral soil and consume decomposed litter and dead roots. These groupings provide an organisational framework that allows the role of earthworms to be characterized in an ecologically meaningful way (Perel, 1979).
Distribution of anecic earthworms in Europe (Lumbricus terrestris and Aporrectodea longa) is not as widespread as that of epigeic and endogeic species (e.g., Dendrobaena octaedra,Aporectodea calliginosa). The distribution of anecic species is limited to the regions dominated by mixed-wood and broad-leaved forests, and the forest-steppe (Perel, 1979) where they are important agents of mull humus form formation. Occurrence of the anecic Lumbricus terrestris has been documented in southern regions of boreal forests, whereas its presence in northern regions is usually associated with anthropogenically disturbed sites (Terhivuo, 1988, Räty and Huhta, 2004).
The various models of earthworm activity that have been developed to date are either population dynamic models or models describing the role in organic matter mineralisation or plant nutrition (Lavelle and Meyer, 1983, Hobbelen and van Gestel, 2007, Pelosi et al., 2008, Ouellet et al., 2008, Johnston et al., 2014, Shashkov et al., 2015), rather than SOM formation. Some models consider the processes of SOM formation by earthworms (Whalen et al., 1999, Blanchart et al., 2009, Huang et al., 2010) but without a link to mesofauna food webs and concepts of humus form development.
The objective of this work was to develop parameters and algorithms to quantify the litter transformation, SOM formation, and release of nitrogen (N) as a module for the Romul_Hum model (Komarov et al., manuscript in preparation [Romul_Hum: problem formulation, model description, and testing]), an improved version of the SOM model ROMUL (Chertov et al., 2001, Komarov et al., 2007). This model is an integral part of the ecosystem model, EFIMOD 2 (Komarov et al., 2003). We started the earthworm module development with anecic earthworms because this group has been intensively studied over the past 150 years, and this work has provided a rich source of published data on their ecology (Perel, 1979, Lee, 1985, Butt, 1993, Baker and Whitby, 2003, Räty, 2004, Shashkov, 2014, Shashkov et al., 2015) and their role in SOM dynamics (Lavelle, 1997, Tiunov and Scheu, 2000, Curry and Schmidt, 2007, Zhang et al., 2013, Edwards et al., 2013, Bouché, 2014). The parameters and algorithms for the anecic earthworm module were developed to be compatible with the approach used to model the role of micro- and meso-biota for the Romul_Hum (Chertov et al., manuscript in preparation [Romul_Hum: parameterisation of food web biota activity]), therefore the population dynamics of earthworms is simplified in the module (total biomass production and death only), and emphasis is put on C and N dynamics. The module should provide a framework for the further elaboration of modules for epigeic and endogeic earthworms and other litter transforming soil macro-fauna (e.g., millipedes, isopods).
Section snippets
The anecic earthworm module of Romul_Hum
The Romul_Hum model (Komarov et al., manuscript in preparation [Romul_Hum: problem formulation, model description, and testing]) was developed to simulate the role of all soil biota, including micro- and meso-fauna (Chertov et al., manuscript in preparation [Romul_Hum: parameterisation of food web biota activity]) and macro-fauna, in the production of stable SOM and available N. Eco-physiological parameters have been documented for the functional groups of earthworms (Striganova, 1980,
Discussion
The set of anecic earthworm functional parameters forSOM formation that we have described here represents an improvement over an existing model of SOM dynamics, ROMUL (Chertov et al., 2001) and was developed specifically for the modified version of this model, Romul_Hum. In the Romul_Hum model, earthworm cast production and processes within casts are combined with micro- and meso-faunal FW activity to directly evaluate their role in the formation of new SOM. The approach that we used for anecic
Conclusion
There is a clear contradiction between historical and modern views of the pedological role of earthworms and their function within ecosystems. In the past, the role of earthworms in humus formation, and in particular mull humus formation, was accentuated (Kubiëna, 1953, Edwards and Bohlen, 1996, Baritz, 2003). Nowadays attention focusses on the high litter mineralisation rate in the earthworm gut through litter disintegration and fusion with the mineral soil and on the role of earthworms in
Acknowledgements
This work was supported by the Program 18 of the Presidium, the Russian Academy of Sciences, and grants 15-04-05400-а, 15-04-08712-а, and 15-04-08707 of the Russian Foundation for Basic Research and the Canadian Forest Service, Natural Resources Canada. We thank Peggy Robinson for careful editorial suggestions.We greatly appreciate feedback from two anonymous reviewers that significant improved the article.
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