(Lumbricus terrestris) and physical, chemical and ...

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Urban Ecosyst DOI 10.1007/s11252-010-0145-4

A microcosm study of the common night crawler earthworm (Lumbricus terrestris) and physical, chemical and biological properties of a designed urban soil Bryant C. Scharenbroch & Douglas P. Johnston

# Springer Science+Business Media, LLC 2010

Abstract Designed soils are used in specialized urban areas, such as under sidewalks or on roof-tops. These substrates have coarse light-weight aggregates to meet load-bearing specifications with soil in voids for rooting medium. A full-factorial microcosm approach was used to study Lumbricus terrrestris (two adult worms added and no-worms added), compaction (bulk density of 1.95 and 1.48 g cm−3), and litter (litter and no-litter additions) in a designed soil. Earthworm biomass, soil physical, chemical, and biological properties, anion leaching and surface C efflux was measured on days 0, 7, 14, 21, 28, 72, 112, and 140. Earthworms decreased bulk density in compacted soil, but did not impact density of un-compacted soil. Earthworm biomass increased days 7 to 14, but declined from days 28 to 140, likely as result of the abrasiveness of the aggregate component and relatively shallow depth of the soil (25 cm). During the period of increasing earthworm biomass, surface C efflux, microbial biomass N, soil Ca2+ and NH4+ increased with earthworms. During the period of declining earthworm biomass, surface C efflux, microbial biomass N, soil Ca2+ and NO3−, and leachate NO3− increased, and soil pH decreased with earthworms. While alive and dying, Lumbricus terrestris stimulated microbial activity and biomass and nutrient availability, but an apparent shift to nitrification was observed as earthworm biomass declined. The results show Lumbricus terrestris to improve designed soil properties for plants, but the improvements may be short-lived due to the inability of these earthworms to survive in the designed soil. Keywords Urban soil . Designed or structural soil . Lumbricus terrestris . Compaction . Nutrient availability . Microbial biomass and activity

B. C. Scharenbroch (*) Research Department, The Morton Arboretum, 4100 Illinois Route 53, Lisle, IL 60532-1293, USA e-mail: [email protected] D. P. Johnston Department of Biological Sciences, University of Illinois at Chicago, 845 West Taylor Street, Chicago, IL 60607, USA

Urban Ecosyst

Introduction Earthworms are important for pedogenesis and have many impacts on soil properties (Edwards 2004). Earthworms have been shown to affect soil physical properties, such as density, structure, aeration, and moisture (Jordan et al. 1999, 2000; Ponder et al. 2000). Chemical properties, such as pH, nutrient availability, and heavy metals are affected by earthworms (Buse 1990; Robinson et al. 1992; Buck et al. 1999; Wen et al. 2006). Earthworms influence microbial composition, biomass, and activity and thus affect the rates and patterns of mineralization and immobilization in soils (Bohlen and Edwards 1995; Binet and Trehen 1992; Binet et al. 1998). Earthworm activity is influenced by many factors, such as food quality and quantity (Lee 1985; Edwards and Bohlen 1992; Curry 2004), temperature and moisture (Berry and Jordan 2001), soil properties (e.g., pH, texture and structure) (Nuutinen et al. 1998; Baker and Whitby 2003), and multitude of biotic interactions (e.g., competition, predation, parasitism, disease, etc) (Edwards 2004). Relationships of earthworms and soil properties have been well-documented for agricultural systems (Baker et al. 1992; Lamande et al. 2003; Decaens et al. 2004; Winsome et al. 2006) and forests (Whalen 2004; Marhan and Scheu 2005; Heneghan et al. 2007). In comparison, few studies have examined the roles of earthworms in urban soils (Steinberg et al. 1997; Smetak et al. 2007). Steinberg et al. (1997) found rural soils with earthworms had significantly higher rates of nitrogen (N) mineralization than urban soil with earthworms and rural soil without earthworms. Smetak et al. (2007) found earthworm density was significantly different among urban park (437 individuals m−2), old residential (121 individual m−2) and young residential sites (26 individual m−2). Decreases in bulk density and increases in carbon (C) and N content were associated with increased earthworm biomass as urban systems age (Smetak et al. 2007). Compared to soils in other environments, urban soils are highly modified (Craul 1985). Soils in urban areas tend to have low organic contents and microbial activities, and high pH values, salt contents, densities, and concentrations of contaminates (Short et al. 1986; Kelsey and Hootman 1990; Scharenbroch et al. 2005; Scharenbroch and Lloyd 2006; Pouyat et al. 2007). As a result of these anthropogenic influences, urban soils tend to be difficult substrates for growing plants (Craul 1999). Designed urban soils are used to integrate infrastructural and plant growth needs in specialized plantings, such as city street tree planters and roof top gardens (Costello and Jones 2003; Oberndorfer et al. 2007). These designed soils, referred to as structural, skeletal, or bimodal, are gap-graded, large aggregate-soil systems. Designed soils consist of approximately 80% coarse aggregate mix, typically 10 to 25 mm diameter, to meet load-bearing specifications and reduce substrate mass (Grabosky and Bassuk 1996). The remaining 20% is typically silt loam or silty clay loam, suspended as a rooting medium within the interconnected voids (Grabosky and Bassuk 1996). Some studies have examined the physical properties of structural soils (Grabosky and Bassuk 1996; Smiley et al. 2006; Grabosky et al. 2009), but research has not been performed on their chemical and biological properties. Lumbricus terrestris (common night crawler) are anecic earthworms, which are large, dorsally-pigmented, feed on litter and soil, dwell in the soil, and create permanent vertical burrows. Lumbricus terrestris produce 38 cocoons per year, reach maturity in three months and complete their lifecycle within six months (Butt 1993). Lumbricus terrestris incorporate large amounts of organic matter deep into the soil, and strongly impact soil organic matter dynamics and nutrient availability (Scheu and Wolters 1991). Numerous studies have reported on the potential of Lumbricus terrestris to invade temperate forests and dramatically impact nutrient storage and availability of these ecosystems (Groffman et al.

Urban Ecosyst

2004; Bohlen et al. 2004; Hale et al. 2005). Lumbricus terrestris have been shown to hasten decomposition of the forest floor, increase nitrogen mineralization, and even facilitate increased abundance of an invasive shrub, Rhamnus cathartica (European Buckthorn) (Heneghan et al. 2007; Madritch and Lindroth 2009). Earthworm populations in designed soils have yet to be described. However, Lumbricus terrestris often dominate urban soils (Steinberg et al. 1997; Smetak et al. 2007). Kennette et al. (2002) found Lumbricus terrestris to survive in and bioaccumulate heavy metals from contaminated urban soils of Montreal. Others report on the ability of Lumbricus terrestris to live in soils amended with sewage sludge (Tomlin et al. 1993; Kizilkaya 2004). Lumbricus terrestris has been identified as a species well-suited for restoration of degraded soils (Butt 1993). A major limiting factor for earthworm survival in designed soils would appear to be moisture. Water constitutes 75 to 90% of the body weight of earthworms (Grant 1955), so the prevention of water loss is essential for survival of earthworms in structural soils with relatively low water holding capacities (Grabosky et al. 2009). Lumbricus terrestris can lose 70% of their total body water (Roots 1956) and have been shown to be able to withstand dry conditions in non-irrigated plots better than other species (Gerard 1960). It is unknown if any species can persist in urban structural soils, but we suspect Lumbricus terrestris may be best suited to these harsh environments. If they can survive, it is likely these worms will have dramatic effects on ecosystem functions, none of which are currently detailed for these unique urban habitats. The first objective of the study was to determine if Lumbricus terrestris would survive in structural soil microcosms, with and without compaction and litter additions. We hypothesized that Lumbricus terrestris would survive in structural soils and based this suspicion on literature demonstrating these worms to be ubiquitous, invasive, and adaptive. The second objective was to determine the impacts of Lumbricus terrestris on physical, chemical, and biological properties of structural soil. We hypothesized Lumbricus terrestris to decrease bulk density, increase microbial activity and biomass, and increase available nutrients in designed urban soil.

Materials and methods Microcosms consisted of cylindrical polyvinyl chloride containers (15 cm diameter by 25 cm height) filled with 1.5 kg of Cornell University Structural Soil™ (CU soil). The depth of the soil in microcosms was selected as a typical depth found in greenroof installations (Dunnett and Nolan 2004). The CU soil was produced with a gravimetric ratio of 80% crushed limestone (12.5 to 25.0 mm range in size aggregrate), 20% silty clay loam and 0.025% hydrogel binder (Gelscape® Amereq. Inc.). Initial properties of silty clay loam fraction were (mean ± standard deviation): pH (7.3±0.1), electrical conductivity (EC) (176.2±10.5 μs cm−1), sodium, Na+ (116.9±2.8 mg kg−1), potassium, K+ (105.2±1.1 mg kg−1), calcium, Ca2+ (418.7± 4.4 mg kg−1); magnesium, Mg2+ (248.9±2.4 mg kg−1); cation exchange capacity, CEC (29.5±1.1 cmol+ kg−1); organic carbon, C (8.8±0.3%); total nitrogen, N (0.2±0.0%); ammonium, NH4+ (4.7±0.9 mg kg−1); nitrate, NO3− (19.2±1.3 mg kg−1); dissolved organic N (DON) (12.4±2.0 mg kg−1); and microbial biomass N (MBN) (53.2±6.9 mg kg−1). Prior to placement, soil was saturated with deionized water and frozen at −25°C for 72 h to eliminate remaining small earthworms and earthworm cocoons (Bohlen and Edwards 1995). The microcosms were set up in a two by two by two experimental design with two compaction treatments (with and without compaction), two litter treatments (with and without litter), and two earthworm treatments (with and without earthworms). There were 15 replicates of each of the eight compaction x earthworm x litter treatment combinations, for a total of 120 microcosms. Three microcosms from each treatment combination were

Urban Ecosyst

destructively sampled at 0, 7, 14, 28, and 140 days following the litter and earthworm additions. During the experiment, microcosms were maintained in a greenhouse at 20°C with light regime of 14 light and 10 hours dark. Soil moisture contents were maintained at 15 to 20% gravimetric moisture content by adding 100 ml of deionized water three times weekly throughout the duration of the experiment. Microcosm bottoms had drainage wicks to collect soil leachates and the tops were equipped for static measurements of surface C efflux. Sixty microcosms were compacted with a standard compaction drop hammer (American Association of State Highway and Transportation Officials, T-99) with 592.7 kJ m−3 effort to 1.95±0.01 g cm−3 (AASHTO 1995). Prior to compaction, the Proctor test was used to determine the optimum moisture content (19±0.5% gravimetric soil moisture) to maximize compaction effort. Sixty additional microcosms were prepared with no compaction effort to 1.48±0.02 g cm−3. Sixty microcosms received 10.0 g of leaf litter, added to the surface, and sixty received no litter. The litter was from a northern hardwood stand, predominantly northern red oak (Quercus rubra), white oak (Quercus alba), sugar maple (Acer saccharum), and red maple (Acer rubrum). The litter was partially decomposed, with particle sizes of 10 to 25 mm, and initial C/N ratios of 45/1±1.7, standard deviation. Immediately following litter additions, two adult Lumbricus terrestris earthworms (4,500 to 6,000 mg each) were added to sixty microcosms. The number of earthworms added was equivalent to a field population density of 113 worm m−2, which is within the density of earthworms reported in urban soils, 50 to 450 earthworms m−2 (Smetak et al. 2007). At each of the five dates, 24 microcosms were sampled. Areas of litter and earthworm casts (cm2) were measured at each sample date by placing a transparent grid on the surface. Bulk density (g cm−3) was calculated by dividing the oven-dried soil weight for each microcosm by its volume (Grossman and Reinsch 2002). Earthworms were separated from the soils by hand, stored in petri dishes for 3 days to remove gut contents, and the total live biomass (mg) was determined for each microcosm. The percent relative change in earthworm biomass was expressed by the mg change in biomass / initial worm weight in mg for each microcosm. All soil from each microcosm was then mixed and sub-sampled for soil characterization. Sub-samples were weighed, dried for 24 h at 105°C, and reweighed to calculate gravimetric soil moisture (%). Total C and N (%) were determined by automated dry combustion with an Elementar Vario EL III CHNOS analyzer (Elementar, Hanau, Germany). Soils were extracted with 1 M NH4OAc (pH 7.0) and mg kg−1 of K+, Ca2+, Mg2+, and Na+ were determined with atomic adsorption spectroscopy (Model A5000, Perkin Elmer Inc., Waltham, MA) (Schollenberger and Simon 1945). The effective cation exchange capacity (CEC) was expressed as the sum of those cations (cmol+ kg−1). Soil pH and electrical conductivity (EC) in μs cm−1 were measured in 1:1 (soil:deionized) water pastes (Model Orion 5-Star, Thermo Fisher Scientific Inc., Waltham, MA). The soil fumigation-extraction method (Brookes et al. 1982; Cabrera and Beare 1993) was used to determine microbial biomass N (MBN) in mg kg−1. Soil sub-samples were fumigated with ethanol-free chloroform for 5 days, extracted with 0.5 M K2SO4, and total extractable N was reduced to NH4+ with persulfate and Devarda’s alloy for NH4+ absorbance readings at 650 nm (Model ELx 800, Biotek Instruments Inc., Winooski, VT) (Sims et al. 1995). Microbial biomass N was the difference in N between the fumigated and unfumigated samples, using an extraction efficiency factor of KEN =0.54 (Joergensen and Mueller 1996). Colorimetric N analyses were also used for determination of dissolved organic N (DON), NO3−, and NH4+ in mg kg−1 in non-fumigated samples (Sims et al. 1995). The 24 microcosms that were destructively sampled on day 140 were used to collect leachates and measure surface C efflux at days 7, 14, 21, 28, 72, 112, and 140. Surface C efflux (mg CO2 m−2 h−1) over 24-h was measured with 0.25 M NaOH traps. Carbon dioxide sequestered in NaOH was precipitated with 0.5 M BaCl2 followed by 0.25 M HCl

Urban Ecosyst

(standardized) titration to a phenolphthalein endpoint (Anderson and Domsch 1978; Parkin et al. 1996). After incubations, microcosms were leached with 150 ml of deionized water. The first 20 ml of microcosm leachates were collected, filtered through quantitative filters (Fisherbrand Q2), and analyzed using ion chromatography for mg kg−1 of Br−, Cl−, F−, NO3−, and SO42− (Metrohm 732-IC detector, 733-IC seperation center, 709 and 752-IC pumps, and Metrosep anion column-dual 1/C 6.1006.020, Metrohm USA Inc. Riverview, FL). Statistical analyses were conducted using SAS JMP 7.0 software (SAS Inc., Cary, NC). Data distributions were checked for normality using the Shapiro-Wilk W test. Attempts were made to transform non-normal data using log10 and natural log transformations. Nonparametric analyses, Mann-Whitney and Kruskal-Wallis, were used to test non-normal data that could not be transformed. Significance of the main effects of earthworms, compaction, and litter on soil properties and processes and the interactions among these main effects (earthworms x compaction, earthworms x litter, compaction x litter, and earthworms x compaction x litter) were analyzed using analysis of variance (ANOVA) and mean separations carried out with Tukey’s HSD tests. Temporal changes were analyzed using repeated measures ANOVA. Significant differences were determined at the 95% confidence level.

Results Effects on earthworm biomass, cast area, and litter area Effects of compaction and litter on earthworm biomass (change in biomass / initial worm weight) were not significant (p≥0.6947) (Table 1). Across all earthworm treatments earthworm biomass increased from days 0 to 14, but decreased during days 28 to 140 (Fig. 1). Earthworm cast area was greater (p=0.0179) for compacted microcosms compared to non-compacted (Table 1). Litter did not impact earthworm cast area (p=0.2011) (Table 1). More (p=0.0049) litter remained on the surface in microcosms without earthworms compared to those with worms (Table 1). Compaction did not impact (p=0.9073) the amount of litter remaining (Table 1). Interaction effects were not significant (p≥0.0773) for the change in earthworm biomass, cast area or litter area (Table 1). Effects of earthworms on CU soil properties Earthworm impacts were detected for soil pH (pF

0.8781





Prob>F

EW*CP







0.4073

0.0197c

0.7978

0.6468

0.0400c