Soil & Tillage Research 194 (2019) 104312

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Soil & Tillage Research

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Camponotus japonicus mounds indirectly accelerate leaf litter decomposition by altering soil temperature and moisture T ⁎ ⁎ Tongchuan Lia,b, Yuhua Jiac, Ming’an Shaoa,b,c,d, , Nan Shena, a State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Yangling 712100, China b Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China c College of Water Conservancy, Shenyang Agricultural University, Shenyang 110866, China d CAS Center for Excellence in Quaternary Science and Global Change, Xi’an 710061, China

ARTICLE INFO ABSTRACT

Keywords: As ecosystem engineers, soil-inhabiting can influence soil properties in different ways. However, limited Bioturbation attention has been directed toward the role of Camponotus japonicus on litter decomposition in the Loess Plateau. Loess Plateau This study quantified the impact of C. japonicus mounds on soil evaporation, temperature and litter decom- Soil evaporation position. The distribution and physical properties of C. japonicus mounds in four slopes (61 m × 5 m) under different vegetation types [Korshinsk peashrub (Caragana korshinskii K.), KOP; purple alfalfa (Medicago sativa L.), ALF; natural fallow, NAF; and millet, MIL] were studied. The density of ant mounds in grass and shrublands was considerably higher than that in croplands. Farming activities and intense soil erosion in the crop slope could play a negative role in mound density. On average, half-ellipsoid ant mounds were 2.48 cm in height and 755 cm2 in basal area with 0.75 g/cm3 bulk density. The size distribution of the ant mounds was as follows: 2–3 (6.9%), 1–2 (27.3%), 0.5–1 (16.9%), 0.28–0.5 (18.2%) and < 0.28 mm (30.7%). Porous ant mounds that cov- ered the leaf litter of ALF reduced soil evaporation, increased soil temperature and indirectly accelerated leaf litter decomposition. Concentrations of soil organic matter (SOC), total N, ammonium N, nitrate N, available P and available K were higher in soil under ant mounds than those in surrounding soil under KOP, ALF and NAF. High soil moisture and temperature in the leaf litter and enhanced contact area between the soil particles and the leaf litter promoted litter decomposition and contributed to the formation of a ‘fertile island’. These findings may enrich our understanding on the effects of ant activity on soil ecosystems in semiarid areas.

1. Introduction surface (Wagner et al., 2004). An ant can form and carry soil pellets as large as its head (Hooper-Bui et al., 2002). Ants use different excavation The substantial increase of vegetation cover across the Loess Plateau strategies for varying water content (from dry to saturated) and make in northwest China (Gao et al., 2017)effectively restrains soil erosion pellets with different microstructures (Espinoza and Santamarina, and promotes the development of ant colonies (De Araújo et al., 2015) 2010). The continuous heaping of soil pellets forms a mound on the soil by providing abundant food and suitable habitats. Earthworms are fa- surface. Ant mounds that cover ant nests are formed from soil pellets, miliar ‘ecosystem engineers’ and are well known for improving soil dead ant bodies and seed hulls discarded by harvest ants (Wagner et al., health (Jouquet et al., 2012). Ants appear to replace earthworms as soil 2004). The scale of an ant mound is linearly correlated with the number ecosystem engineers in dry habitats (Evans et al., 2011). Ants are of worker ants (Li et al., 2017a). Many ant species can build above- ecosystem engineers (Jones et al., 1994) that can affect the structure ground mounds (Dauber and Wolters, 2000; Gorosito et al., 2006; (Tschinkel, 2003), hydrology (Cerdà and Jurgensen, 2008), chemistry Ohashi et al., 2007). The mound of the chaco leafcutter ant ( vol- (Jílková et al., 2011) and biota of soils (Ginzburg et al., 2008). In lenweideri) can reach approximately 1 m in height and 6–7 m in basal contrast to earthworms, the quantitative effects of ant activities on soil diameter (Cosarinsky and Roces, 2007). Ant mounds directly and in- properties in semiarid areas receive less attention. directly affect soil physical characteristics; leaf fragments plug air cir- Soil-inhabiting ants create pores, tunnels and chambers by ex- culation in nest mounds (Bollazzi and Roces, 2007, 2010a). Ants collect cavating soil particles underground and depositing them on the soil leaves to thatch their nests (Bollazzi and Roces, 2010b) and deposit

⁎ Corresponding authors. Present address: No. 26, Xinong Road, Yangling, Shaanxi Province, 712100, China. E-mail addresses: [email protected] (M. Shao), [email protected] (N. Shen). https://doi.org/10.1016/j.still.2019.104312 Received 5 January 2019; Received in revised form 1 June 2019; Accepted 27 June 2019 0167-1987/ © 2019 Elsevier B.V. All rights reserved. T. Li, et al. Soil & Tillage Research 194 (2019) 104312 charcoal litter around nest entrances to alter soil temperature (Smith and MIL. KOP is a native species on the northern Loess Plateau, while and Tschinkel, 2007). In 2016, we investigated the role of ant mounds ALF is a non-indigenous species. In 2004, KOP was planted with a in restricting soil evaporation and regulating the temperature of bare 70 cm × 70 cm row spacing, and ALF was planted with a 50 cm row soil (BS) (Li et al., 2017a). However, most areas in the terrestrial eco- spacing. KOP was left to grow naturally without human interference, system are not bare because fallen leaves cover the soil surface. Ants whereas ALF was harvested twice every year in late July and late Oc- remove soil pellets from underground and transfer them to the top of tober by cutting near the soil surface. NAF developed naturally after the leaf litter mulches. Although ant mounds on the soil surface can alter arable land was abandoned in 2004. The crop plot was weeded twice the physical and chemical properties of underground soil, this phe- during the growing season. The soil in all plots was Aeolian loess. nomenon has yet to be comprehensively studied. Two perpendicular diameters and four heights in all four cardinal Leaf litter can provide plants with nutrients and results in microbial directions were measured on each mound. The above-ground ant production, and litter decomposition plays a key role in the ecosystem mound volumes were calculated by using the half-ellipsoid equation (Duffy, 2002). Numerous factors, such as leaf litter type, temperature, (Risch et al., 2005). On May 25, 2017, the soil around the nest entrance, humidity, acidity and microbes, can greatly affect leaf litter decom- including the ant mound and the soil matrix at 0–2.5 cm depth, was position (Garcia-Pausas et al., 2004; Cornwell et al., 2008; Butenschoen collected and brought to the laboratory. Four ant mounds in different et al., 2011; Martínez et al., 2014). Soil fauna is an important compo- slopes were randomly sampled. Undisturbed samples were used to in- nent in leaf litter decomposition because it can alter decomposition vestigate the soil physical properties, namely bulk density and particle rates and nutrient transformation in many ecosystems (Yang and Chen, composition. Disturbed samples were used to investigate the chemical 2009; Meyer et al., 2011). For example, millipedes, earthworms and properties, namely soil organic matter (SOC), total N, nitrate N, am- affect decomposition by crushing and digesting litter, monium N, available P and available K content. The surrounding soil thereby improving microbial activity (Stadler et al., 2006; Milcu et al., without mounds was also sampled for comparison. 2008). Although the effects of ant activities on soil properties and processes have been assessed (Frouz and Jílková, 2008), the impact of 2.3. Property measurement ant mounds on leaf litter decomposition has yet to be quantitatively investigated. We hypothesised that ant mounds covering leaf litter Soil in the mound was oven dried at 105 °C for 24 h. We used five would distinctly affect soil evaporation and temperature, thereby in- sieves (i.e. 3, 2, 1, 0.5 and 0.28 mm) to classify the pellets and evaluate directly modifying microbial activities which play a significant role in their size distribution. The disturbed soil samples were air dried, cru- litter decomposition. shed and passed through 0.25 mm sieves prior to chemical analysis. The We examined Camponotus japonicus, a species that is widely dis- analytical methods described in the Institute of Soil Science of Chinese tributed on plateaus and has the largest body (10–12 mm in length) Academy of Science (1981) were adopted to determine SOC and total N among ants. This study aimed to (1) investigate the distribution of ant content. SOC was measured through wet digestion with a mixture of mounds and its effects on soil chemical properties in four slopes planted potassium dichromate and concentrated sulphuric acid. Total N was with different vegetation, namely Korshinsk peashrub (Caragana kor- measured using the semi-macro Kjeldahl method. Soil samples were shinskii K.), KOP; purple alfalfa (Medicago sativa L.), ALF; natural fallow, extracted with KCl, and inorganic N (i.e. nitrate and ammonium) con- NAF; and millet, MIL and (2) evaluate the effect of ant mounds and centrations in the extracts were measured using an Alpkem auto-ana- leaves of ALF on soil evaporation, temperature and leaf litter decom- lyser (Pulse Instrumentation, Saskatoon, Saskatchewan, Canada). position. Available P was extracted using NaHCO3, and the colorimetric mea- surements of inorganic P were conducted using the molybdate–ascorbic 2. Materials and methods acid method (Murphy and Riley, 1962). Available K was determined using a flame photometer (Chapman, 1965). 2.1. Study site 2.4. Effects of ant mound on soil evaporation, soil temperature and litter Liudaogou Catchment is in the northern Loess Plateau, approxi- decomposition mately 14 km west of Shenmu County, Shaanxi Province, China. This catchment is located at 110°21′–110°23′E and 38°46′–38°51′Natan Fifteen buckets (20 cm × 20 cm, H × L, with sealed bases) were elevation of 1094–1274 m. The region is characterised by a temperate, used as soil containers in the laboratory to quantify the effects of ant semiarid climate with a mean annual precipitation of 430 mm, of which mound on soil properties. Each iron bucket was filled with 6.3 kg of air- 77% occurs between July and September. The average annual tem- dried and sieved soil. Thereafter, 3.2 kg of water was added to saturate perature is 8.4 °C, and the mean annual potential evapotranspiration is the soil in each bucket. Soil was collected from the bare land with 785 mm (Jia et al., 2013). The study area is situated at the centre of the 0–30 cm layers in the field. A PVC pipe (1.5 cm × 18 cm, D × L; with a water–wind erosion crisscross region (Tang et al., 1993). Soil in this 0.1 cm gap along the pipe) was inserted into the soil to adjust the region suffers from wind erosion in spring and winter and from water gravimetric water content in subsequent experiments. BS without litter erosion in summer and autumn. Croplands were reconverted into for- or pellet layer was set as the control treatment. Treatments with ALF estland, shrublands and grassland to remedy soil erosion in the past leaves (100 g) and different levels of thickness of C. japonicus pellets decade (Jia et al., 2017), which led to intense soil drought (Jia et al., (i.e. 0, 5, 10 and 15 mm; e.g. 0, 120, 240 and 360 g) covering the soil 2019). surface were named M1, M2, M3 and M4, respectively, and conducted in triplicate. Buckets were randomly placed on the ground outside, 2.2. Ant mound investigation and field soil sampling exposed to diurnal cycles of solar radiation and covered with film during precipitation to prevent water addition. Once the gravimetric C. japonicus worker ants expand their nests during early May and soil moisture content was reduced to 20%, which is the soil field ca- late October in the Liudaogou Catchment. After the mating flight, queen pacity, the litter and pellets were placed on the soil surface. As an N- ants fall on the ground and make new nests, which may not develop fixing plant, the leaves of ALF are an important source of soil organic into mature nests in the future. Therefore, on May 2017, before the matter. The fallen leaves of ALF were air dried and used to evaluate the mating flight, we investigated and marked C. japonicus ant mounds in effects of the pellet layer covering the fallen leaves on soil evaporation, the upper, middle and bottom locations of four slopes (5 m × 61 m, temperature and litter decomposition. The buckets were weighed, and 12°–14°) facing the northwest direction (Fig. 1a). The four vegetation water was added until it reached 20% at 6:00 every day for 81 con- types consisted of typical vegetation restoration types: KOP, ALF, NAF secutive days (from July 14, 2017 to October 2, 2017). Each bucket was

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Fig. 1. Experimental slopes (KOP, ALF, NAF and MIL) (A) in the field of Liudaogou Catchment. The ant mound in the bare soil (B) and covering on leaf litter (C). weighed by an electronic scale (measurement range: 0–30 kg, with 1 g 2.5. Statistical analysis precision) (Zhujiang Weighing Apparatus Co., Ltd., Yongkang City, Zhejiang Province, China) to estimate the cumulative evaporation and Prior to statistical analyses, the ANOVA residuals were examined for evaporation rates. normality and homogeneity for all the variables. When the assumption On October 23, 2017, the soil moisture content was adjusted to 20% of homogeneity of variance was not met, data were logarithmically in the 15 buckets at 6:00 by using PVC pipes, and a soil thermometer transformed and analysed. The physical and chemical parameters of ant (with 0.1 °C precision) (Haoyu Electronic Technology Co., Ltd., mounds and habitats under different vegetation in the field were Shenzhen City, Guangdong Province, China) was installed in the leaf compared using two-way ANOVA. No interaction between the mound litter layers of each bucket to monitor the daily variations of soil tem- effects and vegetation effects was considered. One-way ANOVA fol- perature. Air temperature was monitored by temperature sensors ex- lowed by a least significant difference test (P < 0.05) was also con- posed to air. The weight of each bucket and the soil temperature were ducted to examine the effects of ant mounds on soil evaporation, tem- measured every 2 h from 6:00 to 20:00. perature and soil chemical properties among laboratory treatments. All After 81 days of consecutive evaporation, the mulches and the soil statistical analyses were conducted using SPSS 16.0 (IBM Corp., matrix were collected from each bucket at a depth of 0–1 cm to evaluate Armonk, NY). All figures were computed using Origin 8.0 software their effects on litter decomposition. The samples were air dried and (Origin Lab, Northampton, MA) and Photoshop CS6.0 (Adobe Systems passed through a 1 mm mesh to separate leaves from the soil. The re- Corporation, San Jose, US). sidual leaves were washed and air dried to estimate the litter loss rate using the following equation: R (%) = W (g)/12 g × 100%, where R L R L 3. Results is the litter loss rate and WR is the weight of the residual leaves. All the soil samples were air dried, crushed and passed through 0.25 mm sieves Mound density considerably varied among the four treatments at prior to chemical analyses. SOC, total N, nitrate N, ammonium N, − 590, 426, 360 and 131 nest ha 1 for ALF, KOP, NAF and MIL, re- available P and available K were determined in the soil samples. spectively (Table 1). Ant mounds were randomly distributed in the ALF, KOP and NAF slopes but were not found within 18 m from the slope bottom in the MIL treatment. Ant mounds were broadly concave in the four treatments, with an average height of 2.5 cm (1.1–2.9 cm) and

Table 1 Distribution of ant mound and mound size in the slopes under different types of vegetation (KOP, ALF, NAF and MIL). The values are presented as mean or mean ± standard deviation.

Parameters KOP ALF NAF MIL

Mound number 13 18 11 4 − Mound density (ha 1) 426 590 360 131 Mean mound diameter (cm) 32 ± 6 37 ± 5 34 ± 8 36 ± 9 Mean coverage area (cm2) 803 ± 207 1134 ± 175 907 ± 214 1017 ± 223 Total area (cm2) 12,501 17,309 10,577 3846 The ratio of mound area to slope area (%) 0.39% 0.57% 0.35% 0.13% Mean mound height (cm) 2.6 ± 0.3 2.7 ± 0.2 2.4 ± 0.2 2.2 ± 0.4 Mean mound volume (cm3) 697 ± 189 879 ± 156 696 ± 173 746 ± 201

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Table 2 Comparison of physical properties [i.e. size distribution, bulk density (BD) and porosity] between the soil pellets made by using C. japonicus and soil matrix. The values are presented as mean ± standard deviation.

Parameters Pellet diameters (mm) BD (g/cm3) Porosity (%)

< 0.28 (%) 0.28–0.5 (%) 0.5–1 (%) 1–2 (%) 2–3 (%)

Pellet mulch 30.7 ± 2.4 18.2 ± 0.8 16.9 ± 0.9 27.3 ± 2.1 6.9 ± 0.5 0.75 ± 0.06 73.6 ± 3.7 Soil matrix 100.0 0 0 0 0 1.34 ± 0.03 48.5 ± 2.1 diameter of 35 cm (18–43 cm). The mean coverage area of C. japonicus successive hours of evaporation was 64 g, whereas those under the M1, mounds was 965.6 cm2. Nest mounds covered 0.57%, 0.39%, 0.35% M2, M3 and M4 treatments were 32, 21, 16 and 12 g, respectively. The and 0.13% of the slope surface in the ALF, KOP, NAF and MIL, re- evaporation rates reached the maximum values between 12:00 and spectively. No significant difference (P > 0.05) in mound parameters 14:00 (Fig. 2A). The values of the cumulative surface evaporation de- (i.e. mean mound diameter, mean coverage area, mean mound height creased throughout evaporation as the thickness of the ant-made pellets and mean mound volume) was observed among the four treatments. increased (Fig. 2A). Fig. 2B shows the daily soil temperature variation Ant mounds composed of ant-made pellets were placed in five ca- of leaf litter under different treatments and air temperatures. Similar tegories based on diameter: < 0.28, 0.28–0.5, 0.5–1, 1–2 and 2–3 mm. trends were observed in the leaf litter and air temperature. High tem- These pellets were coarser than the particles of the control soil, which peratures were observed in treatments with covering soil pellets (i.e. had a particle diameter less than 0.28 mm. The fraction of the coarse M1, M2, M3 and M4), leading to temperatures higher than that of BS pellets (0.5–3 mm) made by C. japonicus was 51.1% (Table 2). Ap- from 09:00 to 13:00. The presence of numerous pellets resulted in a proximately 6.9% of the pellets were in the 2–3 mm range. The bulk high temperature. The temperatures in M2 (26.6 °C), M3 (28.5 °C) and density of the soil matrix (1.34 g/cm) was significantly (P < 0.01) M4 (30.3 °C) at 11:00 were signifi cantly higher (P < 0.05) than that in higher than that of ant mounds (0.75 g/cm, Table 2). Low soil bulk M1 (25.7 °C). The temperature reached a peak value at 11:00 (Fig. 2B). density of the ant mound (73.6%) led to higher porosity compared with that under the ant mounds (48.5%). 3.3. Effects of ant mound on litter decomposition

3.1. Characteristics of soil nutrients under the ant mound With increasing ant mound thickness, the mean values of mass losses in the leaf litter were 18.3%, 19.5%, 22.1% and 24.3% for M1, The nest mounds had a higher SOC content, total N, ammonium N, M2, M3 and M4, respectively. Soil nutrients positively responded to the nitrate N, available P and available K than those of the surrounding surface mulches of the ant mound. M1, M2, M3 and M4 possessed soils in ALF, KOP and NAF. The difference in SOC content and available significantly higher (P < 0.05) levels of SOC, total N, ammonium N, P between the nest mound and the surrounding soils was significant nitrate N, available P and available K compared with those of BS. The (P < 0.05) in the four treatments (Table 3). The highest SOC content SOC, total N, ammonium N, nitrate N, available P and available K difference between the nest mound and the surrounding soils was ob- concentrations were significantly higher (P < 0.05) in M4 (i.e. 4.47, served in ALF (i.e. 9.36 g/kg vs. 5.41 g/kg). By contrast, the low con- 0.47, 5.56, 1.05, 2.81 and 136.5 mg/kg, respectively) than those in M1 centration of chemical parameters in the nest mounds compared with (i.e. 3.81, 0.41, 4.69, 0.88, 2.59 and 91.5 mg/kg, respectively). that in the surrounding soils was observed in MIL (Table 3). The values However, no significant difference (P > 0.05) in nutrient concentra- of chemical parameters in the nest mounds of ALF, KOP and NAF were tions was observed among M1, M2 and M3. The difference in soil nu- greater than those of MIL (Table 3). However, the levels of SOC, total N, trients between CK and litter mulch treatments without ant mound was ammonium N, nitrate N, available P and available K in the non-mound not significant (P > 0.05) (Table 4). soil of the MIL were significantly higher than those of the other three treatments. 4. Discussion

3.2. Effects of ant mound on daily soil evaporation and temperature The density of ant mounds is greatly affected by climate, topo- graphy, soil, vegetation and external disturbance (Jurgensen et al., Cumulative soil evaporation under BS treatment during the 14 2005; Risch et al., 2005, 2008; Kilpeläinen et al., 2008). Human

Table 3 Chemical parameters (i.e. SOC, total N, ammonium N, nitrate N, available-P and available-K) of ant mounds and the surrounding soil in the slopes under different types of vegetation (KOP, ALF, NAF and MIL). The values are presented as mean ± standard deviation.

Treatments SOC (g/kg) total N (g/kg) ammonium N (mg/kg) nitrate N (mg/kg) available-P (mg/kg) available-K (mg/kg)

KOP With mound 8.13 ± 1.51ab 0.70 ± 0.21ab 8.17 ± 1.76ab 1.64 ± 0.16b 5.81 ± 0.16b 154.1 ± 21.3bc Without mound 5.97 ± 0.77c 0.64 ± 0.16ab 6.97 ± 0.77b 1.50 ± 0.20bc 4.64 ± 0.14c 136.3 ± 11.6 cd ALF With mound 9.36 ± 2.19a 0.66 ± 0.18ab 7.44 ± 1.15b 1.69 ± 0.17b 4.37 ± 0.21c 131.9 ± 18.3 cd Without mound 5.41 ± 0.79c 0.49 ± 0.21b 5.21 ± 0.78c 1.49 ± 0.21bc 3.91 ± 0.12d 118.6 ± 11.9d NAF With mound 8.99 ± 1.05a 0.81 ± 0.19ab 8.09 ± 1.26ab 1.66 ± 0.27bc 4.59 ± 0.17c 168.8 ± 11.9b Without mound 6.19 ± 1.91bc 0.62 ± 0.14b 7.03 ± 1.24b 1.54 ± 0.26bc 3.78 ± 0.24d 143.3 ± 21.6bc MIL With mound 6.39 ± 2.09b 0.59 ± 0.14b 6.83 ± 1.15bc 1.27 ± 0.21c 3.77 ± 0.23d 107.1 ± 20.8d Without mound 9.83 ± 0.56a 0.87 ± 0.09a 9.58 ± 0.88a 3.89 ± 0.42a 6.72 ± 0.11a 186.9 ± 6.8a Vegetation effect F = 0.238 F = 0.774 F = 1.502 F = 2.784 F = 2.538 F = 1.625 P = 0.869 P = 0.523 P = 0.246 P = 0.069 P = 0.087 P = 0.217 Mound effect F = 11.269 F = 0.342 F = 0.453 F = 8.269 F = 9.111 F = 0.284 P = 0.003 P = 0.565 P = 0.509 P = 0.046 P = 0.039 P = 0.601

Statistically homogeneous groups are marked by the same letters (ANOVA, LSD test, P < 0.05). The bottom lines give the results of a two-way ANOVA, mound effect means the effect of mound vs. no-mound; vegetation effect means the effect of KOP, ALF, NAF and MIL compared with each other.

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Fig. 2. Daily variations in the evaporation rates (A) and temperature (B) under four mulch treatments with 100 g of litter and 0 (M1), 5 (M2), 10 (M3) and 15 mm (M4) of pellets compared with bare soil (BS) and air temperature (AT). interference is one of the most important factors that decrease the diffusion from the mound pores to the air. Ant mounds also affect soil density and abundance of mound-building ant species in North America temperature by inhibiting soil evaporation. Latent heat transmitted into (Jurgensen et al., 2005). Clear-cutting action in forests indirectly sup- the air with less evaporation is lower in soil covered by ant mounds presses the boom of insects and is destructive to wood ant colonies than in soil without mound covers, thereby maintaining heat and re- (Kilpeläinen et al., 2008). In the present study, more ant nests were sulting in high temperature in the mound (Li et al., 2017a). In the found in the ALF, KOP and NAF treatments than in the croplands, which present study, the pellet layers helped maintain soil moisture and were highly disturbed by farming activities. Only four nests were found temperature in leaf mulches and soils (Fig. 2). in the cropland, whereas no ant nest or ant mound was found in the Soil moisture and temperature are important factors that control bottom of the crop slope. Intense soil erosion on the bare or crop slope leaf litter decomposition (Scowcroft et al., 2000; Brandt et al., 2010; in the Liudaogou Catchment, situated at the centre of the water–wind Salinas et al., 2011). Changing moisture and temperature dynamics can erosion crisscross region (Tang et al., 1993), is responsible for the ab- alter the proportional contribution of bacteria and fungi to decom- sence of ant colonies or ant nests. The higher mound density in ALF position and soil microbial activity, which mediate critical ecosystem than in other treatments could be due to the sparse inter-vegetation processes (Bell et al., 2008). High soil water availability and soil tem- areas (Willott et al., 2000). In the present work, the mean diameter and perature promote decomposition by increasing the activity of decom- volume of ant mound were approximately 34.8 cm and 754.5 cm3, re- poser communities underneath plant canopies in the forest (Collins spectively, considerably higher than those of Formica sinensis (21.2 cm et al., 2008; Gholz et al., 2000) and result in further nutrient release. In and 346.5 cm3) and Tetramorium caespitum (5.1 cm and 30.6 cm3; per- the present study, porous ant mound delayed evaporation, thereby re- sonal observation). Kilpeläinen et al. (2008) argued that the mean vo- sulting in higher soil moisture content and temperatures than those in lume of Formica aquilonia mounds increases with stand age. However, the BS, a favourable micro-environment for microbes and rapid de- mound size does not depend on environmental parameters, such as composition (Vivanco and Austin, 2006). Ant-made pellets improved precipitation, elevation, slope, aspect and vegetation type (Risch et al., the contact area of the litter to the soil and resulted in a close contact 2008). In the present study, the mound size difference among the four with the microbial communities (Vivanco and Austin, 2006; Berg and treatments was not significant (P > 0.05). McClaugherty, 2013). Ants can carry particles as large as their heads (Hooper-Bui et al., In the present study, soil nutrient concentrations were higher under 2002; Johnson, 2010). The C. japonicus ant mound is made up of soil the mounds than in the surrounding soil in the grass and shrublands pellets, which are much coarser than the sand in the Liudaogou (Table 3). This finding is consistent with the results obtained by Catchment (Li et al., 2017b). Ant-made pellets loosely stacked on the Kristiansen and Amelung (2001). Ant mounds covering the litter could soil surface form ant mounds with low bulk density and high porosity protect leaves from being blown away and the water-soluble nutrients compared with those of the soil matrix (Table 2). Although ant mounds of leaves from drifting because of surface runoff during rainfall. As with are usually drier than the surrounding soil (Ohashi et al., 2007), highly ants in Willott et al. (2000), C. japonicus places soil pellets on BS, which porous ant mounds prevent the rise of capillary water, and vapour in is a nutrient-poor area. Litter accumulation and heaping of ant-made the mound can reduce surface evaporation and contain high soil pellets contribute to the high soil nutrient content under the mound. moisture in the substrate (Li et al., 2017a). Moreover, moisture in the The formation of such small ‘fertile islands’ in the field could change the pores is typically high and can reduce water evaporation from the soil spatial heterogeneity of soil nutrients (Li et al., 2008) and the spatial surface because vapour diffusion in the mound pores is weak (Yuan distribution of plant diversity (Anderson et al., 2004). However, the et al., 2009). The ability of ant mounds to reduce surface evaporation is amount of soil nutrients in the ant mound is much lower than in the greatly correlated to the porosity of the ant mound within a limited surrounding soil of the cropland. This phenomenon may be attributed range (Qiu et al., 2014). Thick mounds lengthen the routes of vapour to the high nutrient content of croplands, which receive annual

Table 4 Litter loss rates, SOC, soil total N, soil ammonium N, soil nitrate N, available P and available K (mean ± SD) measured to evaluate the effects of different thickness levels of ant mound (M1, M2, M3 and M4) on litter decomposition compared with that of BS in the buckets. The symbol “—” means no litter.

Treatments Litter loss rates (%) SOC (g/kg) total N (g/kg) ammonium N (mg/kg) nitrate N (mg/kg) available-P (mg/kg) available-K (mg/kg)

BS – 3.39 ± 0.10c 0.31 ± 0.02b 4.09 ± 0.21c 0.74 ± 0.04c 2.43 ± 0.03c 74.1 ± 7.3c M1 18.45 ± 1.68bc 3.81 ± 0.18b 0.41 ± 0.05a 4.69 ± 0.27b 0.88 ± 0.07b 2.59 ± 0.07b 91.5 ± 10.5b M2 19.57 ± 1.75ab 3.78 ± 0.15b 0.43 ± 0.04a 4.76 ± 0.33ab 0.93 ± 0.05ab 2.72 ± 0.05a 97.4 ± 10.1b M3 22.22 ± 2.41ab 4.23 ± 0.19a 0.45 ± 0.06a 5.37 ± 0.31a 0.92 ± 0.08ab 2.68 ± 0.06ab 118.7 ± 19.4ab M4 24.49 ± 3.56a 4.47 ± 0.21a 0.47 ± 0.08a 5.56 ± 0.44a 1.05 ± 0.09a 2.81 ± 0.09a 136.5 ± 21.7a

Statistically homogeneous groups are marked by the same letters (ANOVA, LSD test, P < 0.05).

5 T. Li, et al. Soil & Tillage Research 194 (2019) 104312 fertiliser application. Worker ants bring a considerable amount of mi- 99, 201–219. neral soil from the deep layers to the surface to mix with soil and have a Espinoza, D.N., Santamarina, J.C., 2010. Ant tunneling-a granular media perspective. Granular Matter 12, 607–616. possible negative role in increasing the soil nutrient in croplands (Frouz Evans, T.A., Dawes, T.Z., Ward, P.R., Lo, N., 2011. Ants and increase crop yield et al., 2003; Holec and Frouz, 2006). in a dry climate. Nat. Commun. 2, 262. Frouz, J., Holec, M., Kalčík, Jiří, 2003. The effect of Lasius niger, (Hymenoptera, Formicidae) ant nest on selected soil chemical properties. Pedobiol. – Int. J. Soil 5. Conclusions Biology 47, 205–212. Frouz, J., Jílková, V., 2008. The effect of ants on soil properties and processes Revegetation in the northern Loess Plateau can increase the density (Hymenoptera: Formicidae). Myrmecol. News 11, 191–199. of ant mounds. Intense erosion in the cropland played a negative role in Gao, H., Pang, G., Li, Z.B., Cheng, S., 2017. Evaluating the potential of vegetation re- storation in the Loess Plateau. Acta Geogr. Sin. 72, 863–874. affecting the density of ant mounds, which had a lower bulk density and Garcia-Pausas, J., Casals, P., Romanyà, J., 2004. Litter decomposition and faunal activity higher porosity compared with the soil matrix. A highly porous ant in Mediterranean forest soils: effects of N content and the moss layer. Soil Biol. – mound covering on leaf litters prevents the rise of capillary water, and Biochem. 36, 989 997. Gholz, H.L., Wedin, D.A., Smitherman, S.M., Harmon, M.E., Parton, W.J., 2000. Long- vapour in the mound can reduce surface evaporation and maintain high term dynamics of pine and hardwood litter in contrasting environments: toward a soil moisture in the substrate. The ability to reduce evaporation is po- global model of decomposition. Glob. Change Biol. 6, 751–765. ff sitively correlated with the thickness of the ant mound. Ant mounds Ginzburg, O., Whitford, W.G., Steinberger, Y., 2008. E ects of (Messor, spp.) activity on soil properties and microbial communities in a Negev Desert eco- help maintain soil temperature by inhibiting soil evaporation and in- system. Biol. Fertil. Soils 45, 165–173. creasing soil temperature. Consequently, ant mounds covering the leaf Gorosito, N.B., Curmi, P., Hallaire, V., Folgarait, P.J., Lavelle, P.M., 2006. Morphological litter indirectly promote litter decomposition. The burrowing activities changes in Camponotus punctulatus (Mayr) anthills of different ages. Geoderma 132, 249–260. of hypogeal ants also improve the micro-environment of the soil surface Holec, M., Frouz, J., 2006. The effect of two ant species lasius niger and lasius flavus on and are vital to seedling establishment. Ants potentially play a positive soil properties in two contrasting habitats. Eur. J. Soil Biol. 42 (Suppl. S1). role in enhancing soil quality in a semiarid ecosystem. Understanding Hooper-Bui, L.M., Appel, A.G., Rust, M.K., 2002. Preference of food particle size among ff several urban ant species. J. Econ. Entomol. 95, 1222–1228. the indirect e ects of ant activities on soil properties and leaf litter Institute of Soil Science of Chinese Academy of Science (ISSCAS), 1981. Soil Chemical and decomposition can provide insights into the mechanisms through which Physical Analysis (in Chinese). Shanghai Science and Technology Publishing House, soil fauna adapts to and alters ecosystems in semiarid areas. In view of Shanghai. the improving vegetation coverage that could provide abundant food Jia, X.X., Shao, M.A., Wei, X.R., Wang, Y.Q., 2013. Hillslope scale temporal stability of soil water storage in diverse soil layers. J. Hydrol. 498, 254–264. and suitable habitats for soil insects, the effects of soil insects on the soil Jia, X., Shao, M., Zhu, Y., Luo, Y., 2017. Soil moisture decline due to afforestation across ecology of the Loess Plateau should be given considerable attention. the Loess Plateau, China. J. Hydrol. 546, 113–122. Jia, X., Shao, M., Yu, D.X., Zhang, Y., Binley, A., 2019. Spatial variations in soil-water carrying capacity of three typical revegetation species on the Loess Plateau, China. Acknowledgement Agric. Ecosyst. Environ. 273, 25–35. Jílková, V., Matějíček, L., Frouz, J., 2011. Changes in the pH and other soil chemical This research was supported by the National Natural Science parameters in soil surrounding wood ant (Formica polyctena) nests. Eur. J. Soil Biol. 47, 72–76. Foundation of China (41530854, 41807011, 41571130081, and Johnson, R.A., 2010. Habitat segregation based on soil texture and body size in the seed- 41571221). harvester ants Pogonomyrmex rugosus and P. barbatus. Ecol. Entomol. 25, 403–412. Jones, G., Lawton, J.H., Shachak, M., 1994. Organisms as ecosystem engineers. Oikos 69, 373–386. References Jouquet, P., Janeau, J.L., Pisano, A., Sy, H.T., Orange, D., Thi, Luu, Nguyet, M., Valentin, C., 2012. Influence of earthworms and termites on runoff and erosion in a tropical Anderson, T.M., Mcnaughton, S.J., Ritchie, M.E., 2004. Scale-dependent relationships steep slope fallow in Vietnam: a rainfall simulation experiment. Appl. Soil Ecol. 61, – between the spatial distribution of a limiting resource and plant species diversity in 161 168. an African grassland ecosystem. Oecologia 139, 277–287. Jurgensen, M.F., Storer, A.J., Risch, A.C., 2005. Red wood ants in North America. Ann. – Bell, C., Mcintyre, N., Cox, S., Tissue, D., Zak, J., 2008. Soil microbial responses to Zool. Fenn. 42, 235 242. temporal variations of moisture and temperature in a Chihuahuan desert grassland. Kilpeläinen, J., Punttila, P., Finér, L., Niemelä, P., Domisch, T., Jurgensen, M.F., Microb. Ecol. 56, 153–167. Neuvonen, S., Ohashi, M., Risch, A.C., Sundström, L., 2008. Distribution of ant spe- ff Berg, B., Mcclaugherty, C., 2013. Plant Litter. Decomposition, Humus Formation, Carbon cies and mounds (Formica) in di erent-aged managed spruce stands in eastern – Sequestration. Springer, Berlin. Finland. J. Appl. Entomol. 132, 315 325. Bollazzi, M., Roces, F., 2007. To build or not to build; circulating dry air organizes col- Kristiansen, S.M., Amelung, W., 2001. Abandoned anthills of Formica polyctena and soil lective building for climate control in the leaf-cutting ant ambiguus. heterogeneity in a temperate deciduous forest: morphology and organic matter – Anim. Behav. 74, 1349–1355. composition. Eur. J. Soil Sci. 52, 355 363. Bollazzi, M., Roces, F., 2010a. Control of nest water losses through building behavior in Li, P.X., Ning, W., He, W.M., Krüsi, B.O., Gao, S.Q., Zhang, S.M., Dong, M., 2008. Fertile ff leaf-cutting ants. Insect Sociaux 57, 267–273. islands under Artemisia ordosica, in inland dunes of northern China: e ects of ha- – Bollazzi, M., Roces, F., 2010b. The thermoregulatory function of thatched nests in the bitats and plant developmental stages. J. Arid Environ. 72, 953 963. South American grass-cutting ant, . J. Insect Sci. 10, 137. Li, T.C., Shao, M.A., Jia, Y.H., 2017a. Characteristics of soil evaporation and temperature Brandt, L.A., King, J.Y., Milchunas, D.G., 2010. Effects of ultraviolet radiation on litter under aggregate mulches created by burrowing ants (Camponotus japonicus). Soil – decomposition depend on precipitation and litter chemistry in a shortgrass steppe Sci. Soc. Am. J. 81, 259 267. ff ecosystem. Glob. Change Biol. 13, 2193–2205. Li, T.C., Shao, M.A., Jia, Y.H., 2017b. E ects of activities of ants (Camponotus japonicus) Butenschoen, O., Scheu, S., Eisenhauer, N., 2011. Interactive effects of warming, soil on soil moisture cannot be neglected in the northern Loess Plateau. Agric. Ecosyst. – humidity and plant diversity on litter decomposition and microbial activity. Soil Biol. Environ. 239, 182 187. ff Biochem. 43, 1902–1907. Martínez, A., Larrañaga, A., Pérez, J., Descals, E., Pozo, J., 2014. Temperature a ects leaf fi Cerdà, A., Jurgensen, M., 2008. The influence of ants on soil and water losses from orange litter decomposition in low-order forest streams: eld and microcosm approaches. – orchards in eastern. J. Appl. Entomol. 132, 306–314. FEMS Microbiol. Ecol. 87, 257 267. Chapman, H.D., 1965. Cation exchange capacity. In: Black, C.A. (Ed.), Methods of Soil Meyer, W.M., Ostertag, R., Cowie, R.H., 2011. Macro-invertebrates accelerate litter de- Analysis. Part 2. America Society of Agronomy, Madison, pp. 891–901. composition and nutrient release in a Hawaiian rainforest. Soil Biol. Biochem. 43, – Collins, S.L., Sinsabaugh, R.L., Crenshaw, C., Green, L., Porras-Alfaro, A., Stursova, M., 206 211. Zeglin, L.H., 2008. Pulse dynamics and microbial processes in aridland ecosystems. J. Milcu, A., Partsch, S., Scherber, C., Weisser, W.W., Scheu, S., 2008. Earthworms and Ecol. 96, 413–420. legumes control litter decomposition in a plant diversity gradient. Ecology 89, – Cornwell, W.K., Cornelissen, J.H.C., Amatangelo, K., Dorrepaal, E., Eviner, V.T., Godoy, 1872 1882. fi O., Westoby, M., 2008. Plant species traits are the predominant control on litter Murphy, J., Riley, J.P., 1962. A modi cation of a single solution method for determi- – decomposition rates within biomes worldwide. Ecol. Lett. 11, 1065–1071. nation of phosphate in natural waters. Anal. Chim. Acta 27, 31 36. Cosarinsky, M.I., Roces, F., 2007. Neighbor leaf-cutting ants and mound-building ter- Ohashi, M., Kilpelainen, J., Finer, L., Risch, A.C., Domisch, T., Neuvonen, S., Niemela, P., ff mites: comparative nest micromorphology. Geoderma 141, 224–234. 2007. The e ect of red wood ant (Formica rufa group) mounds on root biomass, Dauber, J., Wolters, V., 2000. Microbial activity and functional diversityin the mounds of density, and nutrient concentrations in boreal managed forests. J. For. Res. 12, – three different ant species. Soil Biol. Biochem. 32, 93–99. 113 119. fl De Araújo, Ademir S.érgio Ferreira, Eisenhauer, N., Nunes, Luís Alfredo Pinheiro Leal, Qiu, Y., Xie, Z., Wang, Y., Ren, J., Malhi, S.S., 2014. In uence of gravel mulch stratum – Leite, L.F.C., Cesarz, S., 2015. Soil surface-active fauna in degraded and restored thickness and gravel grain size on evaporation resistance. J. Hydrol. 519, 1908 1913. lands of northeast brazil. Land Degrad. Dev. 26 (1), 1–8. Risch, A.C., Jurgensen, M.F., Schuetz, M., Page-Dumroese, D.S., 2005. The contribution of Duffy, J.E., 2002. Biodiversity and ecosystem function: the consumer connection. Oikos red wood ants to soil C and N pools and CO2 emissions in subalpine forests. Ecology

6 T. Li, et al. Soil & Tillage Research 194 (2019) 104312

86, 419–430. administration way of wind-water erosion crisscross region and Shenmu experi- Risch, A., Jurgensen, M.F., Storer, A., Hyslop, M., Schuetz, M., 2008. Abundance and mental area on the Loess Plateau. Res. Soil Water Conserv. 2, 2–15. distribution of organic mound‐building ants of the Formica rufa group in Yellowstone Tschinkel, W.R., 2003. Subterranean ant nests: trace fossils past and future? Palaeogeogr. National Park. J. Appl. Entomol. 132, 326–336. Palaeoclimatol. Palaeoecol. 192, 321–333. Salinas, N., Malhi, Y., Meir, P., Silman, M., Cuesta, R.R., Huaman, J., Farfan, F., 2011. The Vivanco, L., Austin, A.T., 2006. Intrinsic effects of species on leaf litter and root de- sensitivity of tropical leaf litter decomposition to temperature: results from a large- composition: a comparison of temperate grasses from North and . scale leaf translocation experiment along an elevation gradient in Peruvian forests. Oecologia 150, 97–107. New Phytol. 189, 967–977. Wagner, D., Jones, J.B., Gordon, D.M., 2004. Development of harvester ant colonies alters Scowcroft, P.G., Turner, D.R., Vitousek, P.M., 2000. Decomposition of Metrosideros soil chemistry. Soil Biol. Biochem. 36, 797–804. polymorpha leaf litter along elevational gradients in Hawaii. Glob. Change Biol. 6, Willott, S.J., Compton, S.G., Incoll, L.D., 2000. Foraging, food selection and worker size in 73–85. the seed harvesting ant Messor bouvieri. Oecologia 125, 35–44. Smith, C., Tschinkel, W., 2007. The adaptive nature of non-food collection for the Florida Yang, X.D., Chen, J., 2009. Plant litter quality influences the contribution of soil fauna to harvester ant, Pogonomyrmex badius. Ecol. Entomol. 32, 105–112. litter decomposition in humid tropical forests, southwestern China. Soil Biol. Stadler, B., Schramm, A., Kalbitz, K., 2006. Ant-mediated effects on spruce litter de- Biochem. 41, 910–918. composition, solution chemistry, and microbial activity. Soil Biol. Biochem. 38, Yuan, C., Lei, T., Mao, L., Liu, H., Wu, Y., 2009. Soil surface evaporation processes under 561–572. mulches of different sized gravel. Catena 78, 117–121. Tang, K.L., Hou, Q.C., Wang, B.K., Zhang, P.C., 1993. The environment background and

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