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Exploring the world beneath your feet : soil mesofauna as potential biological indicators of success.. Battigelli, Jeffrey P. 2011

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Proceedings - Tailings and Mine Waste 2011 Vancouver, BC, November 6 to 9, 2011  Exploring the World Beneath your Feet – Soil Mesofauna as Potential Biological Indicators of Success in Reclaimed Soils Jeffrey P. Battigelli* Stantec Consulting, Sidney, BC Canada *previously with Paragon Soil & Environmental, Edmonton, AB Canada  Abstract Soil formation is crucial for successful reclamation of industrial affected land. Companies are anxious to obtain ecological data indicating success of their remediation efforts. Soil fauna are a vital part of soil ecosystem function, actively involved in decomposition, nutrient cycling and soil formation. Soil mesofauna are an abundant and species-rich group of organisms in soil that may also provide a useful function as biological indicators of habitat disturbance, soil quality and reclamation success. The primary objective of this study was to compare soil mesofauna communities among natural and reclaimed sites and establish baseline data to allow for long-term monitoring of recolonization on disturbed sites. Reclamation prescription significantly influenced density and community structure of soil mesofauna. Densities were greater in natural soils than in reclaimed soils and community structure differed between natural and reclaimed soils. Integration of this biological data with other monitored soil properties should provide a better overall indication of soil ecosystem recovery and reclamation success.  Introduction Soils are a non-renewable natural resource vital for productivity in the terrestrial environment (Lavelle 1996). Chemical and physical properties of soils have been studied intensively for many years. Although soil organisms are considered to have a critical role in soil development (Pawluk 1985) and maintaining soil fertility (Seastedt 1984), the biological component of soils has been largely ignored in North America. The density, diversity and ecological roles of soil organisms in most North American forest soil ecosystems are poorly understood due to a lack of intensive studies and the development of baseline information (Kevan 1985, Marshall 1993). Species diversity of soil organisms rivals that of a coral reef (Wallwork 1970). All major animal phyla are represented in the soil, except for Coelenterata and Echinodermata (Hole 1981). Hundreds of species, represented by thousands or millions of individuals, can occupy a single square meter of soil (Battigelli et al. 1994, Moldenke 1990). The soil ecosystem has been variously referred to as ‘the poor-man’s tropical rainforest’ (Giller 1996, Usher et al. 1979) and ‘the other last biotic frontier’ (André et al. 1994). These organisms may also provide a useful function as bioindicators of soil health (Wallwork 1988, Hogervorst et al. 1993, Linden et al. 1994, Pankhurst et al. 1995, van Straalen and Verhoff 1997). Soil fauna activity is also used in soil humus classifications (Green et al. 1993) and precise species identification could characterize different soil types (Rusek 1989). Rombke et al. (2005) suggested that protecting soil ecosystem biodiversity would contribute to maintaining the functional sustainability of the soil ecosystem. Collection of baseline data on the density, diversity and distribution of soil fauna is essential in order to utilize this community as biological indictors of soil health and monitor changes in disturbed ecosystems (Behan-Pelletier 1999).  Proceedings - Tailings and Mine Waste 2011 Vancouver, BC, November 6 to 9, 2011  Several studies have examined the effectiveness of reclamation efforts and the recolonization of various soil fauna groups on mining spoils and tailings (Hutson 1980, Luxton 1982, Parsons & Parkinson 1986, Cuccovia & Kinnear 1999, Wanner & Dunger 2002). Mites and springtails, commonly referred to as mesofauna, represent a numerically abundant and species-rich group of organisms in the soil. These organisms respond quickly to changes in the soil habitat and may also provide a useful function as bioindicators of habitat disturbance and soil quality (Hogervorst et al. 1993, Pankhurst et al. 1995, van Straalen & Verhoff 1997). In fact, changes to faunal assemblages may be detected prior to changes in physical or chemical properties, thus making soil fauna useful indicators of successful or detrimental reclamation activities (Garay & Nataf 1982). Companies are anxious to obtain ecological data indicating the success of their remediation efforts (St. John et al. 2002). Integration of biological with chemical and physical information can provide ecological data to monitor the performance of reclaimed land sites and indicate the success or failure of remediation efforts (Bagatto & Shorthouse 1999). Since these organisms are a vital part of soil ecosystem function, an understanding of the diversity, density and distribution of these organisms is important especially in light of the reclamation efforts being used on the oil sands areas in northern Alberta. The primary objective of this study was to survey and compare the structure, density and diversity of the soil mesofauna community on natural and reclaimed sites and establish baseline data on soil mesofauna to enable long-term monitoring of recolonization by this community on disturbed sites.  Methods Site descriptions Sample sites were located around the Fort McMurray area including undisturbed, natural plots south and north of town and reclaimed plots located within mine sites boundaries of Syncrude, Suncor and Albian Sands. The area is characterized by a continental boreal climate with long, cool winters and short, cool summers. Mean daily temperatures range from -18.8oC in January to 16.8oC in July (Environment Canada 2011). Annual precipitation is 455 mm, predominately rain (342 mm) during the summer months. The area is within the Boreal Forest Region and forest vegetation includes white spruce (Picea glauca (Moench) Voss), black spruce (Picea mariana (Mill.) BSP), trembling aspen (Populus tremuloides Michx.), balsam poplar (Populus balsamifera L.), white birch (Betula papyfrifera Marsh.), and jack pine (Pinus banksiana Lamb.) as the main tree species (Fung and Macyk 2000). Most soils in the area developed on glacial and post-glacial deposits with Gray Luvisols associated with till and lacustrine deposits and Dystric Brunisols present in coarser parent material such as glaciofluvial outwash and eolian sands (Turchenek and Lindsay 1982, Lanoue 2003).  Study descriptions For this study, samples were collected from previously established long-term soil and vegetation (LTSV) plots located in both reclaimed and natural areas around Fort MacMurray, Alberta. In the reclaimed areas, six reclamation prescriptions were evaluated in this study: (1) PM/SEC/TSS; (2) DP/TSS; (3) PM/SEC/OB; (4) DP/OB; (5) PM/TSS; and (6) PM/OB. Peat mineral mix (PM) is a mixture of peat and mineral materials obtained by over stripping peat into mineral soil. Secondary material (SEC) is surficial geological material salvaged to a depth where the material is considered to be of poor quality for plant growth. Direct Placement (DP) refers to suitable quality soil or surficial geological material taken from a natural deposit and placed directly on tailings sand or overburden. Tailings sand (TSS) is the fine sand material which is one of the final products of the hydrocarbon removal process and Overburden (OB) is the material obtained from below the soil profile and extends to the ore deposit. Natural sites included a-, b-, d- and e- ecosites. The a-ecosite presents dry, rapidly drained, acidic soils with coarse-textured, glaciofluvial parent materials. The forest floor is usually covered by bearberry and lichen with bog cranberry and blueberry also present. Jack pine stands dominate the ecosite. The b-ecosite has the same coarse textured parent materials but tends to be moister and more nutrient rich than a-ecosites. The forest floor contains plant species similar to a-ecosites as well as low-bush cranberry, dewberry and wild sarsaparilla with  Proceedings - Tailings and Mine Waste 2011 Vancouver, BC, November 6 to 9, 2011  jack pine, green alder and aspen present in the forest canopy. The d-ecosite is nutrient poor with imperfectly to poorly drained soils. Acidic soil conditions are reflected by the presence of Labrador tea and bog cranberry over top of fine-textured morainal or glaciolacustrine parent materials. Black spruce dominates most mature stands. The e-ecosite is wet and nutrient rich, commonly found on fluvial or glaciolacustrine parent materials. Organic matter accumulates in these ecosites and combined with high water tables, enhances the nutrient supply (Beckingham and Archibald 1996). In total 65 LTSV plots were selected for sampling. Three soil cores (4.5 cm ∅ x 5 cm deep) were randomly collected from each plot during each of three sampling trips: Summer 2004 (soil temperature of 10 oC at 10 cm), Fall 2004 (leaf colour change in trembling aspen) and Spring 2005 (bud burst on trembling aspen). In addition to standardizing sampling times among sites, these seasonal indicators relate to biological activity in the soil and span the range of seasonal variation in distribution and life stages for soil fauna at these sites. Soil cores were placed in a modified Merchant-Crossley extractor for seven days. Specimens were extracted into specimen cups containing ethylene glycol. Specimens were rinsed with water through a 54 µm sieve until no ethylene glycol remained. Sieve contents were backed washed with water into watch glasses for sorting and counting under a dissecting microscope. Specimens were identified to the following levels: Acari (mites) to suborder, Collembola (springtails) to family and the remaining specimens to class, order or family level depending on the group. Sorted material was stored in 70% ethanol. Density (number of individuals/sample) and relative abundance ([number of individuals per taxon/total individuals collected] x 100) were used in the analyses. Density is useful for estimating population size and determining changes in absolute abundance while relative abundance is useful to compare distribution patterns of taxa and the similarity of these patterns among sites, seasons or horizons (Wallwork 1976). Only taxa with an overall relative abundance >1% of all collected material were considered for further analyses. Data were divided into two groups for analysis: coarse- and fine- textured soils. Coarse textured soils included a- and b- ecosites and reclamation prescriptions using TSS. Fine textured soils included d- and e- ecosites and reclamation prescriptions using overburden (OB) materials. For both groups data were transformed to meet assumptions of normality before analyses. Density data were log transformed [log10 (X+1) where X = actual count of individuals/sample for a taxon] and relative abundance data were arcsine transformed (arcsin √p where p=relative abundance of the taxon). One-way Analysis of Variance within each reclamation prescription was used to compare pooled reclamation treatments to natural ecosite values within soil texture groups (α=0.05). If significant differences were recorded then Holm-Sidak Method was used for a multiple comparison procedure. If data violated ANOVA assumptions, then a Kruskal-Wallis one-way ANOVA on ranks was done followed by Dunn's Test if significant differences were recorded. SigmaPlot 11 (build by Systat Software Inc. was used for all statistical procedures.  Results Sandy Soils Densities in natural sites with sandy soils averaged around 120,000 individuals/m2and densities in reclaimed sites raged from 47,000 to 95,000 individuals/m2. Densities of soil mesofauna were significantly greater in becosites than in any of the reclamation prescriptions while densities in a-ecosites were significantly greater than densities in the PM/SEC/TSS or DP/TSS prescriptions but not PM/TSS prescriptions (Figure 1).  Proceedings - Tailings and Mine Waste 2011 Vancouver, BC, November 6 to 9, 2011  Community structure differed significantly among sites (Figure 2). Proportions of Acari were significantly greater in b-ecosites than any reclamation prescription while values of Acari in a-ecosites were higher than those in DP/TSS and PM/TSS reclamation prescriptions. Proportions of Prostigmata were significantly lower in b-ecosites than all other plots while values for Mesostigmata were significantly higher in PM/SEC/TSS than all other plots. Oribatida values differed significantly between natural ecosites which were both significantly greater than any of the reclamation prescriptions. Furthermore, DP/TSS values were significantly greater than those in PM/SEC/TSS and PM/TSS. Collembolan proportions were reversed with DP/TSS and PM/TSS values being significantly higher than a-ecosite values. Sminthuridae values were significantly lower on b-ecosites than all other plots. Hypogastruridae values were significantly higher on PM/TSS than all other plots. Entomobryidae values were significantly lower on b-ecosites than all others and DP/TSS values for Entomobryidae were significantly greater than a-ecosites, PM/SEC/TSS and PM/TSS. Values of Isotomidae were significantly greater in reclaimed sites, specifically PM/SEC/TSS and DP/TSS, than natural sites (Figure 2).  Fine Soils Densities in natural sites with fine soils ranged from 88,000 to 136,000 individuals/m2. In reclaimed sites using overburden (OB), values ranged from 84,000 to 114,000 individuals/m2. Densities of total mesofauna were significantly greater in d-ecosites than e-ecosites, PM/SEC/OB and DP/OB. Values from e-ecosites did not differ significantly from the reclamation prescriptions examined (Figure 3) Community structure in fine soils followed a pattern similar to sandy soils. Proportions of Acari were significantly lower in e-ecosites and PM/SEC/OB plots than d-ecosites, DP/OB or PM/OB (Figure 1d). Values were also significantly higher in PM/OB and d-ecosites than in DP/OB. Oribatida proportions differed significantly between the two natural sites but values in both natural sites were significantly greater than any reclamation prescription. Conversely, Prostigmata values were significantly greater in all the reclamation prescriptions than in either natural ecosite. Mesostigmata proportions were significantly greater in DP/OB plots than in d-ecosites, PM/SEC/OB and PM/OB but e-ecosites values were significantly greater than PM/OB prescriptions (Figure 4) For Collembola, proportions were significantly lower in PM/OB than all other treatments and decosites values were also significantly lower than e-ecosites, PM/SEC/OB and DP/OB plots. Entomobryidae values were significantly greater in PM/SEC/OB and DP/OB than in PM/OB and both natural plots. Hypogastruridae values were significantly greater in natural sites than in any reclamation prescription. Isotomidae values were significantly lower in PM/OB than either of the natural plots or PM/SEC/OB plots (Figure 4).  Discussion Densities of soil mesofauna ranged from a low of 47, 000 individuals/m2 in reclaimed soils to a high of 136,000/m2 in natural, undisturbed d-ecosites. Densities values in the natural, undisturbed soils fall within the range of values presented from other studies in boreal forest regions (Petersen and Luxton, 1982). Densities tended to be higher in natural ecosites than in reclaimed sites with the exception of PM on either TSS or OB where densities were 95,000and 114,000 respectively. Direct placement and the use of secondary material resulted in lower mesofauna densities relative to natural sites in sandy soils and with fine soils particularly in comparison to natural d-ecosites. Reduced densities are expected in disturbed and reclaimed habitats but overall numbers tell only part of the recovery story on these sites.  Proceedings - Tailings and Mine Waste 2011 Vancouver, BC, November 6 to 9, 2011  Community structure differed significantly between natural, undisturbed ecosites and the different reclamation prescriptions sampled for this study. Although the pattern remains the same with mites dominating the soil mesofauna community in both sandy and fine soils followed by springtails, there is a shift in community structure between natural and reclaimed sites. In sandy soils, proportions of mites are lower in reclaimed plots while values for springtails increase. These differences involve two groups of mites, Oribatid and Prostigmata and several families of springtails including Entomobryidae, Hypogastruridae and Isotomidae. Andres and Mateos (2006) examined the response of several mesofauna taxa and found springtails and oribatid mite species diversity and community structure were the best mesofauna parameters to evaluate soil restoration techniques in Europe. Oribatid mites are one of the most abundant taxa of soil arthropods (Wallwork 1983, Norton 1990) with densities reaching several hundred thousand individuals per square meter in organic horizons (Petersen and Luxton 1982, Battigelli et al. 1994). Roughly 7,000 species of oribatid mites have been described worldwide, representing more than 1000 genera belonging to more than 150 families (Balogh and Balogh 1992) and all closely tied to soil habitats (Norton 1990). Behan-Pelletier (1993) listed 435 species of oribatid mites in Canada with 44 species found in Alberta. Oribatida are “k-selected’ organisms that are long-lived, with low metabolic rates and slow development times. Although this inhibits their ability to take advantage of rapid changes in food resources, low metabolic rates enable them to survive periods with low food intake (Mitchell 1977). Coupled with limited dispersal ability, oribatid mites cannot easily escape impacts or disturbances which usually results in species loss (Behan-Pelletier 1999). There are several species of mites that are disturbance specialists including Oppiella nova and Tectocepheus velatus. Both species are able to recover quickly after a disturbance. This is due to their ability to reproduce parthenogenetically. Higher densities of these species can indicate a recent disturbance event. The impacts of pollution (van Straalen and Verhoef 1997) and silvicultural (Wallwork 1983, Battigelli 2000) and agricultural (Behan-Pelletier 1999, 2003) practices on oribatid mite density and species diversity have frequently been examined. General results include the loss of both density and diversity of oribatid mites in these disturbed areas. Siepel (1995) has suggested that using life history tactics (i.e. feeding habits, reproductive strategies etc.) of oribatid mites could permit comparisons between effects of disturbance and pollution in different biotopes and countries. Collembola are similar in size to oribatid mites and feed on decaying vegetation and microbes. Collembola are relatively well known taxonomically, with an estimated 80% of North American species described (Christiansen and Bellinger 1998). A checklist of Collembola by Skidmore (1995) listed 412 species in Canada of which 55 species were found in Alberta. They are ‘r-selected’ organisms with higher fecundity, faster development and higher reproductive rates than oribatids. Collembola respond more rapidly than most oribatid species to disturbance or nutrient pulses. Several ecological factors, including water content, soil pH, base saturation, Ca, Mg, Mn, and K, and organic matter accumulation have been correlated with collembolan species density and diversity (Hågvar and Abrahamsen 1984, Pozo 1986, Blair et al. 1994, Geissen et al. 1997). A combination of several factors (i.e. vegetative cover, soil type, moisture, temperature, nutrient status, etc.) may influence collembolan density and diversity in any particular habitat with the relative importance of each factor varying for each species. While collembolan density cannot always be correlated with vegetation type (Wood 1966, Curry 1978, Al-Assiuty et al. 1993), several studies have shown that tree species can also influence collembolan densities (Blair et al. 1994, Pinto et al. 1997, Baumbrough 1999).  Proceedings - Tailings and Mine Waste 2011 Vancouver, BC, November 6 to 9, 2011  Goals for soil protection are mainly maintenance of soil quality and soil quantity. By maintaining biological diversity we can assure life support functions of soil. Soil organisms provide objective metrics for biological soil quality, integrating physical, chemical, and biological variables (Blakely et al. 2002). Soil mesofauna play a variety of functional roles in soil processes and contribute to the maintenance of soil fertility (Seastedt 1984), influence bacterial and fungal biomass via grazing, liberating immobilized nutrients and stimulating further fungal and bacterial activity enhancing plant growth (Parkinson 1988, Setälä 1995), transport microbial propagules and spores into new substrates (Kethley 1990, Norton 1990) and contribute to the development of soil structure and humus formation through the deposition of fecal pellets (Pawluk 1985, Hendrix et al. 1990). As bioindicators, these organisms can provide an integrative measure of soil conditions and of a particular soil’s response to disturbance (Wallwork 1988, Hogervorst et al. 1993, Linden et al. 1994, Pankhurst et al. 1995, van Straalen and Verhoff 1997). This fauna is important to soil function, has high species diversity and responds to habitat change. Furthermore, the group has a high density of organisms and great species diversity which can be easily and readily collected from soil samples. Soil arthropods are efficient indicators of ecosystem maturity and can be used in conservation planning and land reclamation monitoring (Andres and Mateos 2006). Analyzing Collembola and Oribatida community data using multivariate methods detected differences between natural and restored soils and Andres and Mateos (2006) concluded that Collembola and oribatid mite species diversity may be useful indicators for forest soil recovery. However, use of Acari and Collembola as indicators of soil quality is in early stages of development in Canada (Behan-Pelletier 2003). Use of soil mesofauna presents several challenges such as total diversity, establishing standardized sampling, collection and extraction methodologies, seasonality of invertebrate fauna, and establishing the existence of rare or endangered invertebrate species associated with rare and unique habitats (Greenslade 2007). Most of these difficulties can be resolved provided proper resources are in place. While invertebrate data can provide an indication of the degree of re-establishment of ecosystem functioning, more work needs to be done to relate ecosystem function to soil organism diversity, density and distribution.  Conclusions Soil fauna represents a large, diverse group of organisms that influence and are affected by soil chemical and physical properties. They are intimately involved with a variety of essential soil processes and functions including organic matter decomposition, nutrient cycling and soil structure development. A better understanding of this community, its structure and its relationship to various soil processes would enhance our understanding of how the soil system works. Further research, development and integration of soil chemical, physical and biological properties, will develop a fuller understanding of the functioning of the below ground ecosystem. Process studies examining decomposition rates, nutrient transfer (i.e. labeled nutrients such C and N) in the soil, soil formation, soil structure and LFH development all provide an opportunity to integrate data to determine the response of different parameters and how each property may be linked to others. Use of monitoring programs will assist in evaluating the impacts of various natural and anthropogenic disturbances on various soil properties and provide the potential to assess the effectiveness of management and rehabilitation programs. These monitoring programs may also help determine which reclamation practice/technique is most effective. Soil mesofauna would be useful for assessing disturbance over time and for comparing different management practices since this group is very specious, has high densities in the soil and respond to impacts in the soil habitat. Standardized sampling methodology in all programs is critical to enable comparison of results among different sites and  Proceedings - Tailings and Mine Waste 2011 Vancouver, BC, November 6 to 9, 2011  treatments. Using soil mesofauna as Indicators can integrate biological, chemical and psychical properties of the environment, this can be interpreted beyond the information that the measured parameter represents by itself (species numbers). Soil mesofauna are linked to ecosystems processes and responsive to variations in management and climate on an appropriate time scale (Doran and Safley, 1997). Developing standard sampling and analysis protocols would enable comparisons of community structures among different forest types and reclamation prescriptions provincially, nationally and globally. No single approach is feasible to assess soil quality at present. The main problem is a lack of baseline data for comparison. Further research is required to develop data from natural soils of various ages and various ecosites to enable comparisons among data sets from recovering ecosites that are disturbed, either natural (i.e. fires, slides, storms, etc.) or as a result of anthropogenic (logging, agriculture, mining, etc.) activities. Analyses include a comparison of life history strategies (r vs. k) and lists of species for multivariate statistical analyses comparing reference areas with disturbed areas. Eventually a master list consisting of species and associated environmental variables (i.e. soil fertility, chemical and physical properties, vegetation community) can be developed to enable the evaluation of soil arthropod communities in reclaimed soil. Comparing this fauna with soil arthropod communities in natural soils of various ages should be able to determine if reclamation is proceeding in the correct direction. There is great opportunity to integrate data on soil biological properties with data of soil chemical and physical properties. This will develop a keener sense of overall soil function and recovery from disturbance and various reclamation practices. Ideally this identifies species assemblages of soil fauna to incorporate soil fauna diversity, distribution and community structure into decision support systems for reclamation procedures.  References Al-Assiuty, A.I., Bayoumi, B.M, Khalil, M.A., and van Straalan, N.M. 1993. 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Primary immigration and succession of soil organisms on reclaimed opencast coal mining areas in eastern Germany. European Journal of Soil Biology, 38:137-143. Wood, T.G. 1966. The fauna of grassland soils with special reference to Acari and Collembola. New Zealand Ecological Society Proceedings, 13: 79-85. Petersen, H. and Luxton, M. 1982. A comparative analysis of soil fauna populations and their role in decomposition processes. Okios, 39:287-388.  Proceedings - Tailings and Mine Waste 2011 Vancouver, BC, November 6 to 9, 2011  Figure 1:  Mean density of total soil mesofauna (individuals x 103/m2) (+SE) in sandy textured soils by site. (Columns with same letter are not significantly different).  Figure 2:  Mean relative abundance of soil mesofauna (%) in sandy textured soils by site. (Groups with out or with same letters are not significantly different)  Proceedings - Tailings and Mine Waste 2011 Vancouver, BC, November 6 to 9, 2011  Figure 3:  Mean density of total soil mesofauna (individuals x 103/m2) (+SE) in fine textured soils by site. (Columns with same letter are not significantly different).  Figure 4:  Mean relative abundance of soil mesofauna (%) in fine textured soils by site. (Groups with out or with same letter are not significantly different).  


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