Geoderma 348 (2019) 158–167

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Geoderma

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Camponotus japonicus burrowing activities exacerbate soil erosion on bare T slopes c,⁎ a,b,d,⁎⁎ a Tongchuan Lia,b, Yuhua Jia , Ming'an Shao , Nan Shen 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, Key Laboratory of Soil Erosion Control and Ecological Restoration in Liaoning Province, Shenyang Agricultural University, Shenyang 110866, China d College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100190, China

ARTICLE INFO ABSTRACT

Handling Editor: Morgan Cristine L.S. As soil ecosystem engineers, ants considerably affect soil physical and chemical properties, and further ac- ff ff Keywords: cordingly a ect soil erosion. However, few study was made on studying the e ects of ant-burrowing activities on Ant mound soil erosion previously. This study quantified the impacts of ant (Camponotus japonicus)-burrowing activities on Rainfall simulation runoff and soil erosion rates. Simulated laboratory rainfall experiments were undertaken on six soil tanks filled Soil erosion rate with clay-loam soil classified as a cumulic anthrosol, three of which introduced with ant colonies for two days − Runoff rate and the other three were without ant colonies, under 40, 80, and 120 mm h 1 of rainfall intensities and a slope fi − Water in ltration of 15°. Results showed that ants made mounds with a bulk density of 0.75 g cm 3, which was lower than that of − the soil matrix, i.e. 1.34 g cm 3. Soil erosion rates for the tanks with ants were 6.78, 36.90, and − − − 62.00 g m 2 min 1 under three rainfall intensities of 40, 80, and 120 mm h 1, which were much higher than − − those of 3.94, 23.49, and 44.48 g m 2 min 1 for the tanks without ants. Ant nests reduced the runoff rate by 31%, 20% and 13% compared with those without ants and enhanced the soil water storage within 90 cm depth. Ant nests played a positive role in soil water conservation due to the large nest entrance diameter and the continuous macropore network. However, the ant mounds provided a loose erodible material and changed micro-topography of the slope surface, thereby accelerating the rill formation and exacerbating soil erosion. This study can help understand the effects of burrowing insects on soil erosion, which is an important environmental problem on the Loess Plateau.

1. Introduction Loess Plateau and can make nest entrances with large diameters (4.1–6.6 mm) (Li et al., 2017a). Ant nests can be 10 cm to almost 4 m Ants are present in almost all terrestrial ecosystems (Liu et al., 2010) deep and are akin to underground fortresses (Tschinkel, 2003). These and are ecosystem engineers (Jones et al., 1994) that can affect the depths are much greater than those of other insects, such as mole structure (Tschinkel, 2003), hydrology (Cerdà and Jurgensen, 2008), crickets (64.1 cm) (Bailey et al., 2015) and dung beetles (20–30 cm) chemistry (Jílková et al., 2011) and biota of soils (Ginzburg et al., (Brown et al., 2010). 2008). The burrowing activities of ants dramatically alter the physical Some studies focused on the effects of ant nests on the infiltration of properties of soil at a small scale. Ant colonies are able to create water and solutes (e.g. Cerdà and Jurgensen, 2008; Li et al., 2014). abundant macropores, galleries, and chambers within their nests Large-diameter tunnels can create high levels of water infiltration (Karlen et al., 2003). Nest size depends on the body type of ants, colony (Eldridge, 1993). Owing to the large nest entrance diameter and the scale and ant species. The species of ants herein is Camponotus japonicus, continuous macropore network of C. japonicus nests (Li et al., 2017a), which has the largest body (10–12 mm long) among ants found on the rainfall can quickly flow into the soil (Bailey et al., 2015). Burrows with

⁎ Correspondence to: Y. Jia, College of Water Conservancy, Key Laboratory of Soil Erosion Control and Ecological Restoration in Liaoning Province, Shenyang Agricultural University, Shenyang, 110866, China. ⁎⁎ Correspondence to: M. Shao, Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China. E-mail addresses: [email protected] (Y. Jia), [email protected] (M. Shao). https://doi.org/10.1016/j.geoderma.2019.04.035 Received 28 October 2018; Received in revised form 8 April 2019; Accepted 18 April 2019 0016-7061/ © 2019 Elsevier B.V. All rights reserved. Y. Jia, et al. Geoderma 348 (2019) 158–167 large tunnels also have a large contact area between nests and soil, The soil tank (2 m long, 0.5 m wide, and 1.0 m deep) is shown in thereby increasing infiltration capacity. Li et al. (2014) demonstrated Fig. 1. The tank had 351 holes (0.5 cm in diameter) at the bottom to that ant-induced soil disturbance can increase the amount of soil water facilitate drainage. Prior to packing the tank, the soil water content of at 40–100 cm deep by enhancing infiltration in areas covered by bio- the tested soil was determined and used to calculate how much soil was − logical soil crusts in the arid desert ecosystems of China. With such needed and to obtain the target bulk density of 1.35 g cm 3, which was high-level infiltration, ant nests can cause only a small amount of sur- similar to that in the field. First, a 5 cm thick layer of sand was packed face runoff at the fine scale (Li et al., 2014). Within a landscape, ant at the bottom of the tank to allow free drainage of excess water. During nests also increase the heterogeneity of infiltration rates and alter sur- the packing process, the soil layer was packed in 10 cm increments. face hydrological processes (Cammeraat and Risch, 2008). Second, the tanks were flatly exposed to rainfall and solar radiation for Ants can further create spherical soil pellets and carry them onto the a month to ensure that the simulated soil water conditions in the tanks soil surface with their mandibles when burrowing a nest. These pellets are similar to those in the field. Prior to the experiments, the slope of are stacked around the nest entrance and form a mound that is rela- the soil tank was adjusted to 15°. Three pipes (100 cm long and 2.8 cm tively stable when the wind blows. In dry season, ant mounds can re- in diameter) were installed in the soil (Fig. 1) to measure soil water duce soil evaporation (Li et al., 2017b), similar to artificial mulching contents at depths of 10, 20, 30, 50 and 90 cm with a PR2–6 probe such as gravel, sand, cobble, basaltic tephra and soil biocrust covering (Cambridge, UK, Delta-T Device Ltd.). No pre-rain was conducted to (Diaz et al., 2005; Ma and Li, 2011). However, unconsolidated soil saturate the surface soil before rainfall. Two soil tanks (with and brought to the surface by ants can also increase the potential for soil without ants) were used in each rainfall event. Each treatment was loss (Cerdà and Jurgensen, 2008). Ant-made pellets (Li et al., 2017b) conducted once; thus, six soil tanks were prepared in total. can easily be hydrolysed and they lead to soil detachment during heavy rains (Cerdà and Doerr, 2007). Many ant species can build aboveground 2.3. Source of test ants mounds or anthills on the soil surface (Ohashi et al., 2005; Kilpelainen et al., 2007). The mounds created by the chaco leafcutter ant (Atta The ants used in this study were collected from several C. japonicus vollenweideri) can considerably affect surface hydraulic processes and nests in the field of Yangling City through a field survey. We dug the sediment transport (Cerdà and Jurgensen, 2008, 2011). However, re- soil along the tunnels of ant nests using a small shovel. Once the nests search that quantitatively evaluates the effects of ant-burrowing ac- were destroyed, soldier and worker ants emerged to defend the nests tivities on runoff and soil loss remains lacking. and were collected using a modified dust catcher. After the slope of the In this study, three simulated rainfall experiments were conducted soil tank was adjusted to 15°, 12 colonies with 200 worker ants in each to (1) quantify the effects of ant-burrowing activities on soil water colony were collected and introduced into the tanks. We considered no content profile, runoff rate and soil erosion rate under different rainfall significant difference in nest volume among the plots with an equal intensities and (2) explore the mechanism through which ant bur- number of worker ants introduced into soils. Four PVC cylinders (40 cm rowing activities affect soil loss. diameter and 20 cm height) were evenly laid onto the soil surface of each tank. A colony was introduced into each PVC cylinder. To prevent 2. Materials and methods ants from escaping, talcum powder was smeared on the inner wall of each cylinder. Damp soil was easy to burrow, and the ants constructed 2.1. Rainfall simulator and lived in their nest for two days.

A rainfall simulation system was used to apply rainfall in the rain- 2.4. Experimental measurements fall-simulation laboratory of the State Key Laboratory of Soil Erosion and Dryland Farming in Yangling City, Shaanxi Province, China. This We collected and dried soil pellets made by ants in an oven at 105 °C simulator can be set to any selected rainfall intensity ranging within for 24 h. The pellets were placed in a measurement cylinder without − 30–150 mm h 1 by adjusting the nozzle size and water pressure (Shen compaction to estimate the bulk density of the ant mounds. Five sieves − et al., 2016). Three rainfall intensities (40, 80, and 120 mm h 1) were (3, 2, 1, 0.5 and 0.28 mm) were used to classify the pellets, which were applied in the experiments. The fall height of the raindrops was 18 m then oven-dried and weighed to determine the size distribution. above the ground, which allowed all raindrops to reach terminal ve- Rainfall experiments were subsequently conducted. The designed locity prior to impact with the soil surface (Zhou et al., 2002). Ad- rainfall amounts were applied to the soil tanks. For each treatment, the ditionally, the simulated raindrop could successfully replicate natural time of runoff initiation was recorded, and runoff samples were col- raindrop size and distribution. A total rainfall amount of 80 mm was lected in 5 L buckets as runoff occurred. The samples were measured at maintained in each treatment for the three designed rainfall intensities. 2 min intervals throughout the entire rainfall duration, with 120 min for − − − − Thus, the rainfall durations were 120 min for 40 mm h 1, 60 min for 40 mm h 1, 60 min for 80 mm h 1, and 40 min for 120 mm h 1, re- − − 80 mm h 1, and 40 min for 120 mm h 1. spectively. The collected samples were allowed to stand for 12 h. The clear supernatant was discarded and the wet soil was oven-dried at 2.2. Preparation of soil and tank 105 °C and weighed to calculate the soil erosion rate. After the simu- lated rain, the tanks were covered with plastic mulch to reduce eva- Soil was collected from the bare land of 0–50 cm layers in Xibo poration. After 24 h, a PR2–6 probe was used to measure the soil water Village (34°20′N, 108°24′E; 521 m above sea level) of Yangling, Shaanxi content profiles in the tanks. Then, we dug the soil along the ant tunnels Province, China. The area is characterized as a semi-humid zone with a to measure the nest depth and entrance diameter. mean annual precipitation of 637 mm and a mean annual temperature of 12.9 °C (Li et al., 2004). The collected soil was air dried and passed 2.5. Data analysis through a 2 mm sieve to remove small stones and weeds. Soil particle sizes were analysed by laser diffraction with a Mastersizer 2000 (Mal- Soil erosion rate and runoff rate were calculated with the following vern Instruments, Malvern, England). The potassium dichromate oxi- equations: – dation external heating method was used to analyse soil organic matter W (Nelson and Sommers, 1982). The soil organic matter and particle size Er = AT× (1) distribution are shown in Table 1. The soil used in this study was the – fi D V clay loam soil, which is classi ed as cumulic anthrosol (FAO/UN- R = × 103 ESCO). T AT× (2)

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Table 1 Details of soil organic matter content and particle-size fractions of sand, silt, and clay for the test soil. Values are presented as the mean ± standard deviation.

Parameters 2–0.02 mm (%) 0.02–0.002 mm (%) < 0.002 mm (%) Organic matter − (g kg 1)

Values 39.6 ± 2.1 36.1 ± 2.4 24.3 ± 1.5 3.6 ± 0.3

Roces, 2012). Even small colonies of Trachymyrmex turrifex, consisting of only two or three dozen individuals, build a single cylindrical turret that is 1–4 cm high (Wheeler, 1907). However, mounds made by C. japonicus workers have no turret to improve ventilation or prevent the inflow of runoff during rainy periods (LeBrun et al., 2011). They do not need extra ventilation because they construct tunnels with 6 mm dia- meter in soils. In addition to the deposition of excavated soil pellets around nest entrances that form a nest mound (Robinson et al., 2008), a number of ant species transport materials from the surroundings to the mound surface (Smith and Tschinkel, 2005), and these materials may be used to stabilize the mound structure, provide protection from erosion (Whitford, 2003), or control heat or humidity exchanges with the en- vironment (Bollazzi and Roces, 2010). In the current study, C. japonicus workers simply deposited soil pellets around the nest entrance in the most economical way without constructing functional mounds. Ants can handle particles as large as their heads to form soil pellets (Hooper- Bui et al., 2002; Johnson, 2010). The preferred particle size depends on the mandible size and ant species (Dostál et al., 2005). In the current study, workers of C. japonicus made and carried soil pellets with 2–3 mm diameter, and these pellets are similar to those made by Atta Fig. 1. Tank (2.0 m long, 0.5 m wide, and 1.0 m deep) used to evaluate the vollenweideri grass-cutting ants (pellets with 1–2.8 mm diameter) in the effects of ant burrowing activities on soil moisture and soil erosion process. study of Cosarinsky and Roces (2012). The size distribution of pellets made by C. japonicus was as follows: 2–3 (6.9%), 1–2 (27.3%), 0.5–1 − − – where Er stands for soil erosion rate (g m 2 min 1); W denotes the dry (16.9%), 0.28 0.5 (18.2%) and < 0.28 mm (30.7%) (Table 2). The soil weight of the sediment (g); A is the projected area of the slope (m2; pellets were coarser than the sand particles in northern Loess Plateau in equal to slope area*cos15°); T refers to the sampling duration (min; i.e. China (Li et al., 2017a). By contrast, the pellet diameter carried by M. − 2 min in this study); R stands for runoff rate (mm min 1); D is runoff aciculatus and T. caespitum is < 2 mm (not shown in the tables). In ff depth (mm); V is runoff volume (m3) for each sample. addition to ant type, soil moisture also considerably a ects pellet size. The soil water contents were measured thrice, and the mean values Ants remove soil particles and form loose pellets at a very low water and standard deviation were used to analyse the effects of ant nests on content; with increased water content, particles group to form large and soil water content profiles. Soil water storage (SWS; mm) was calcu- stable pellets (Espinoza and Santamarina, 2010). θ 3 −3 ff C. japonicus workers loosely stacked soil pellets on the soil surface lated from the k (cm cm ; where k refers to di erent soil depths in − and formed mulches with a much lower bulk density (0.75 g cm 3) cm). The SWS values within 90 cm were calculated as follows: − than the soil matrix (1.34 g cm 3, Table 2). Leite et al. (2018) also SWS(0–90 cm)=++++ 100( θ10 θ 20 1.5 θ 30 3 θ 50 2.5 θ 90 ) (3) found that the nest-building activity of the ant Dinoponera quadriceps fi Comparisons of the soil water profiles of the various treatments signi cantly reduces soil bulk density in their mounds in forest and were analysed by a one-way analysis of variance, followed by Fisher's pasture regions. Decreased bulk densities result from increased porosity ff least significant difference (LSD) test (P < 0.05) with SPSS 16.0 (IBM (Collo et al., 2010). The mound porosity of C. japonicus reached 73.6% Corp., Armonk, NY, USA). Origin 8.0 software (Origin Lab, in the present study (Table 2). The samples showed similar porosities of – Northampton, ME, USA) and Photoshop CS 6.0 were used to create the approximately 50% 60% in the study of Cosarinsky and Roces (2012). figures. To build a steady ventilating shaft, Atta vollenweideri worker ants water the interior walls, which exhibit a compact structure with approxi- mately 20% porosity. Meanwhile, ant mounds are compacted by rain- 3. Results and discussion drops, and soil pellets made by ants disintegrate when it rains (Jouquet et al., 2012). After undergoing hydrolysis, the pellets turn into fine soil 3.1. Physical characteristics of ant mounds particles and porosity remarkably decreases (Li et al., 2017b). In the present study, the mound porosity of C. japonicus after the simulated The ant-made pellets that covered the nest entrance created a rainfall experiments (Fig. 2C and D) decreased to 45% (not shown in pancake-like mound on the flat ground (Fig. 2A). The amount of soil the tables). pellets carried onto the soil surface by ants was highly correlated with Although the ant mounds provided a source of loose soil and in- the number of introduced ants (Li et al., 2017b). The mound height and creased the erodible material, a physical crust formed and protected the diameter were 2 and 20 cm, respectively, on the slopes of the tanks in mound from further erosion during rainfall (Fig. 2C). Ant workers also this study. The mound area coverage in the tanks averaged 25% with enlarged their nests, carried pellets from the subground to the surface four introduced ant colonies (Fig. 2B), whereas the control treatments and renewed the mound after rains (Fig. 2F). Porous mounds con- were free of ant mounds. The mound of the chaco leafcutter ant (Atta sistently existed on the soil surface and altered the micro-topography. vollenweideri) can reach approximately 1 m height and 6–7 m basal diameter (Cosarinsky and Roces, 2007). Many ant species construct ventilated turrets in their mounds (LeBrun et al., 2011; Cosarinsky and

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Fig. 2. Pancake-like mound on flat ground (A). Ant colony with 200 worker ants and the queen ant introduced into the tanks (B). Ant mound after rainfall (C) and the − reverse side (D). The rill after rainfall of 120 mm h 1 for 40 min (E). Renewed pellets covering the surface next to the nest entrances on the slope (F).

3.2. Effects of ant-burrowing activities on runoff and soil loss rainfall can quickly flow into soil. In the current work, the values of runoff rate in the treatments with The runoff rates for the control treatments (Fig. 3A, B and C) were ant mounds in the early stage of simulated rainfall were much lower − 0.61, 0.67 and 0.74 mm min 1 on average, which were 31%, 20% and than those in the control treatments (Fig. 3A–C). We attributed this 13% higher than those for the plots with nests (0.47, 0.56 and phenomenon to the preferential water flow in ant nests and dry soil − − 0.66 mm min 1 under rainfall intensities of 40, 80, and 120 mm h 1, pellets on the surface. Ant mounds, which are made of loose soil pellets, respectively). The nest entrances remained open and retained the cap- easily dry upon exposure to sunlight (Li et al., 2017b) and can absorb ability to capture water due to the large entrance diameter of the C. more rainfall than the soil matrix. The infiltration rate decreased as the japonica nest (4.1–6.6 mm). The ant nests had a strong effect on in- nests and mounds became wet and saturated. Thus, the runoff rate in- creasing water infiltration and thus decreased the surface runoff at a creased distinctly with time for the treatment with ant nests. By con- low rainfall intensity. Similarly, Bailey et al. (2015) reported that water trast, the runoff rate series for control plots were steady (Fig. 3A–C). infiltration in plots with a large amount of mole cricket tunnelling is Although ant nests can increase water infiltration, the soil loss in the 12% greater than that in areas with no active mole cricket tunnelling. treatments with ants was higher than that in the control treatments Macropores are the preferential pathways for the movement of most (Fig. 3D–F). The presence of ant mounds increased the soil erosion rate − − water to deep soil (Bailey et al., 2015). The presence of additional (average of 6.78, 36.90, and 62.00 g m 2 min 1) compared with those − − macropores provided by nest entrances leads to additional infiltration (3.94, 23.49, and 44.48 g m 2 min 1) in the control treatments. These and helps reduce runoff at a small scale (Léonard et al., 2004). More- results are consistent with those of previous studies that revealed that over, Eldridge (1993) measured steady-state infiltration and observed a the presence of ant mounds is associated with increased sediment positive relationship between the size of the nest entrance and steady- transport (Cerdà et al., 2009; Cerdà and Doerr, 2010; Cerdà and state infiltration rates. Owing to the large nest entrance diameter of C. Jurgensen, 2011). Ant-mounding activity has a substantial potential japonica nests (Li et al., 2017a) and the continuous macropore network, contribution to soil erosion. The soil pellets created by ants on the soil

Table 2 Comparison of physical properties (size distribution, bulk density, and porosity) between ant mound made by Camponotus japonicus and soil matrix. Values are presented as the mean ± standard deviation.

Parameters Pellet diameters (mm) BD Porosity (g cm−3) (%) < 0.28 (%) 0.28–0.5 (%) 0.5–1 (%) 1–2 (%) 2–3 (%)

Ant mound 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

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− − Fig. 3. Variation in runoff rate (A–C) and soil erosion rate (D–F) during rainfall of 40 mm h 1 for 120 min (A and D), 80 mm h 1 for 60 min (B and E), and − 120 mm h 1 for 40 min (C and F) at 2 min intervals in the tanks with ants and without ants. surface easily become wet and can be washed away by runoff during the treatments with ants than that in the control treatments. Moreover, intense rainfall. However, several researchers have detected an even ant members enlarged their nests after rainfall (Li et al., 2017b). With lower soil erosion rate in areas prone to ant activity, as explained by renewed pellets covering the slope surface (Fig. 2F), mounds always increased infiltrability and lower surface runoff compared with ant-free existed around the nest entrances and increased the sediment output in control areas (Cerdà and Jurgensen, 2008). The ant mound was partly succeeding rainfall events. washed away in the current study. Ant mounds remained on the slope Vegetation plays a positive role in reducing soil erosion (Quinton − (Fig. 2C) even after rainfall intensities of 120 mm h 1 for 40 min. The et al., 1997; Zhang et al., 2015). Little movement of unconsolidated soil raindrops compacted the ant mounds and formed a crusting layer in ant mounds occurs in areas with high vegetation and litter coverage (Fig. 2C). With the protection of crusts on the mound surface, the (Cerdà and Jurgensen, 2008). However, the effects of ant mound on soil pellets under the crust were intact and retained their porous structure erosion cannot be ignored when surface vegetation is removed by in- − (Fig. 2D) with a bulk density of 1.01 g cm 3. The ant mounds changed tensive herbicide use, after wildfire or under steep slopes with heavy the surface micro-topography on the slope and the path of water flow rains (Cerdà et al., 2009; Cerdà and Doerr, 2010; Schmidt et al., 2014). on the soil surface. They promoted the confluence of surface water and On the Loess Plateau of China, the high density of vegetation results in thus accelerated the generation of rill (Fig. 2E), which is an important severe drought and the formation of a dry soil layer (Wang et al., 2010), type of soil erosion (Lu et al., 2016). We considered that rills on the which could lead to regional vegetation loss. In view of the negative slopes were the main factor that caused the higher sediment output in effects of ants on soil erosion in this study, additional studies should be

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− Fig. 4. Soil moisture profiles at soil depths of 10, 20, 30, 50, and 90 cm before and after rainfall of 40 mm h 1 for 120 min in control treatments (A–C) and treatments with ants (D–F).

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− Fig. 5. Soil moisture profiles at soil depths of 10, 20, 30, 50 and 90 cm before and after rainfall of 80 mm h 1 for 60 min in control treatments (A–C) and treatments with ants (D–F).

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− Fig. 6. Soil moisture profiles at soil depths of 10, 20, 30, 50 and 90 cm before and after rainfall of 120 mm h 1 for 40 min in control treatments (A–C) and treatments with ants (D–F).

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Table 3 Variation in soil water storage (SWS; in millimeter) within 90 cm soil depth in the upper, middle, and bottom plots in the treatments without ants and with ants after − − − rainfall of 40 mm h 1 for 120 min, 80 mm h 1 for 60 min, and 120 mm h 1 for 40 min.

− − − Treatments Plots 40 mm h 1 80 mm h 1 120 mm h 1

Before rain After rain Increment Before rain After rain Increment Before rain After rain Increment

Without ant nests Upper 177.3 187.2 9.9 182.6 185.4 2.8 193.8 198.6 4.8 Middle 180.8 192.5 11.7 185.7 188.8 3.1 185.1 189.6 4.5 Bottom 183.3 198.3 15.0 182.8 196.0 13.3 194.9 203.6 8.7 Mean 180.5 192.6 12.2 183.7 190.1 6.4 191.2 197.2 6.0 With ant nests Upper 180.4 195.0 14.6 178.5 192.3 13.8 178.6 185.0 6.4 Middle 182.6 210.7 28.1 212.9 236.2 23.3 184.8 196.2 11.3 Bottom 180.0 234.2 54.2 188.2 217.2 29.1 193.2 219.0 25.8 Mean 181.0 213.3 32.3 193.2 215.2 22.1 185.5 200.0 14.5 conducted to evaluate the risk of soil erosion in the field with ants. and thus improve soil water condition.

3.3. Soil water content profile 4. Conclusion

The water distribution in the soil profile and soil water storage The results suggested that ants play positive and negative roles in within 90 cm for each plot was used to evaluate the contribution of ant changing runoff and soil erosion, respectively. The effects of ant-bur- nests to soil moisture (Figs. 4–6 and Table 3). After rainfall of rowing activities on runoff rate, soil erosion rate and soil water storage − 40 mm h 1 for 2 h, the soil water contents at 0–20 cm depth of each varied considerably under different rainfall intensities. With large dia- plot considerably increased (Fig. 4). Similar to the situation for earth- meters of 4.1–6.6 mm, C. japonicus nests can increase water infiltration worms and other hypogeal social insects (Bailey et al., 2015), the pre- and reduce the runoff rate. Ant mounds contribute to sediment pro- ferential water-flow formation in ant nests can enhance the water duction by providing a readily erodible material and changing the content in deep layers because of the formation of preferential flow in micro-topography on the soil surface. The ant mounds still existed on nest tunnels (Li et al., 2017a). Water infiltration is strongly related to the slope with crusting on the mound surface even under a rainfall − the length of the vertical tunnels (MacMahon et al., 2000). In the pre- intensity of 120 mm h 1. Ant mounds promoted the confluence of sent study, although the mean nest depth was 35.5 cm, the soil water surface water, thereby accelerating the generation of rill and greatly content at 0–50 cm depth for plots with ant nests after rainfall was increasing the sediment output on bare slopes. Considering vegetation much higher than that before rainfall (P < 0.05), particularly in the degradation due to soil desiccation in semiarid areas, the risk of soil bottom plot (Fig. 4F). The preferential flow reached the bottom of these erosion caused by burrowing ants should be a focus of attention. nests and that the water continued to infiltrate. The mean values of the increment in SWS within 90 cm depth in the Acknowledgements − treatments with ants after rainfall of 40, 80, and 120 mm h 1 were 32.3, 22.1, and 14.5 mm (Table 3), respectively, and were much higher This research was supported by the National Natural Science than those (12.2, 6.4, and 6.0 mm, respectively) in the control treat- Foundation of China (41807011 and 41530854), and China ments. With an equal rainfall amount, a lower rainfall intensity pro- Postdoctoral Science Foundation funded project (2018M631562). duced more infiltration and a lower runoff rate (Fig. 3A–C). The ant − nests intercepted less water flow during rainfall of 120 mm h 1 than References − during rainfall of 40 and 80 mm h 1. The reduced infiltration resulted in a shallower infiltration depth and a smaller increment in SWS Bailey, D.L., Held, D.W., Kalra, A., Twarakavi, N., Arriaga, F., 2015. Biopores from mole – crickets (Scapteriscus spp.) increase soil hydraulic conductivity and infiltration rates. (Figs. 4 6 and Table 3). – fi Appl. Soil Ecol. 94, 7 14. Water in ltration depends on nest structure (MacMahon et al., Bollazzi, M., Roces, F., 2010. Control of nest water losses through building behavior in 2000). Tschinkel (2003) argued that each ant species establishes a nest leaf-cutting ants (Acromyrmex heyeri). Insect. Soc. 57, 267–273. with approximately vertical tunnels connecting approximately hor- Brown, J., Scholta, C.H., Janeau, J.L., Grellier, S., Podwojewski, P., 2010. Dung beetles fi (Coleoptera Scarabaeidae) can improve soil hydrological properties. Appl. Soil Ecol. izontal chambers. Chambers are usually vertically strati ed, thereby 46, 9–16. providing various temperature and humidity conditions for food sto- Cammeraat, E.L.H., Risch, A.C., 2008. The impact of ants on mineral soil properties and rage and larva feeding (Mikheyev and Tschinkel, 2004). Large nest processes at different spatial scales. J. Appl. Entomol. 132, 285–294. ff fi Cerdà, A., Doerr, S.H., 2007. Soil wettability, runo and erodibility of major dry- tunnels and chambers can create high levels of water in ltration and Mediterranean land use types on calcareous soils. Hydrol. Process. 21, 2325–2336. storage. For mature C. japonicus nests, the entrance diameter and mean Cerdà, A., Doerr, S.H., 2010. The effect of ant mounds on overland flow and soil erod- chamber area are 4.1–6.6 and 1600 mm2 (Yang et al., 2018), respec- ibility following a wildfire in eastern Spain. Ecohydrology 3 (4), 392–401. Cerdà, A., Jurgensen, M., 2008. The influence of ants on soil and water losses from orange tively, which can contribute to forming a more rapid preferential flow orchards in eastern Spain. J. Appl. Entomol. 132, 306–314. and more water storage than the nests of small ants. The status of nest Cerdà, A., Jurgensen, M.F., 2011. Ant mounds as a source of sediment on citrus orchard entrances also affects the infiltration of water flow. In the current work, plantations in eastern Spain. A three-scale rainfall simulation approach. Catena 85, – the nest entrances remained open throughout a rainfall event. Several 231 236. Cerdà, A., Jurgensen, M.F., Bodi, M.B., 2009. Effects of ants on water and soil losses from ant species (Acromyrmex landolti and Aphaenogaster barbigula) construct organically-managed citrus orchards in eastern Spain. Biologia 64 (3), 527–531. turrets at nest entrances to prevent water infiltration into their nests Colloff, M.J., Pullen, K.R., Cunningham, S.A., 2010. Restoration of an ecosystem function and protect the colony against flooding (Eldridge, 1993; LeBrun et al., to revegetation communities: the role of invertebrate macropores in enhancing soil water infiltration. Restor. Ecol. 18, 65–72. 2011). However, soil pellets excavated by C. japonicus did not impede Cosarinsky, M.I., Roces, F., 2007. Neighbor leaf-cutting ants and mound-building ter- water infiltration due to the broad soil distribution on the top of the soil mites: comparative nest micromorphology. Geoderma 141, 224–234. surface. The worker ants laid pellets in a downward direction next to Cosarinsky, M.I., Roces, F., 2012. The construction of turrets for nest ventilation in the grass-cutting ant Atta vollenweideri: import and assembly of building materials. J. the nest entrances on the slope (Fig. 2F), which can save labour for the Insect Behav. 25, 222–241. ant colony when making their nests and does not block the nest en- Diaz, F., Jimenez, C.C., Tejedor, M., 2005. Influence of the thickness and grain size of trance. C. japonicus nests can act as runoff sinks during rainfall events tephra mulch on soil water evaporation. Agric. Water Manag. 74, 47–55.

166 Y. Jia, et al. Geoderma 348 (2019) 158–167

Dostál, P., Březnová, M., Kozlíčková, V., Herben, T., Kovář, P., 2005. Antinduced soil under aggregate mulches created by burrowing ants (Camponotus japonicus). Soil Sci. modification and its effect on plant below-ground biomass. Pedobiologia 49, Soc. Am. J. 81, 259–267. 127–137. Liu, R.T., Zhao, H.L., Zhao, X.Y., 2010. Effect of vegetation restoration on ant nest- Eldridge, D.J., 1993. Effect of ants on sandy soils in semi-arid eastern Australia: local building activities following mobile dune stabilization in the Horqin Sandy land, distribution of nest entrances and their effect on infiltration of water. Aust. J. Soil northern China. Land Degrad. Dev. 20, 562–571. Res. 31, 509–518. Lu, J., Zheng, F.L., Li, G.F., Bian, F., An, J., 2016. The effects of raindrop impact and Espinoza, D.N., Santamarina, J.C., 2010. Ant tunneling-a granular media perspective. runoff detachment on hillslope soil erosion and soil aggregate loss in the Mollisol Granul. Matter 12, 607–616. region of Northeast China. Soil Tillage Res. 161, 79–85. Ginzburg, O., Whitford, W.G., Steinberger, Y., 2008. Effects of harvester ant (Messor, Ma, Y.J., Li, X.Y., 2011. Water accumulation in soil by gravel and sand mulches: influence spp.) activity on soil properties and microbial communities in a Negev desert eco- of textural composition and thickness of mulch layers. J. Arid Environ. 75, 432–437. system. Biol. Fertil. Soils 45, 165–173. MacMahon, J.A., Mull, J.F., Crist, T.O., 2000. Harvester ants (Pogonomyrmex spp.): their Hooper-Bui, L.M., Appel, A.G., Rust, M.K., 2002. Preference of food particle size among community and ecosystem influences. Annu. Rev. Ecol. Syst. 31, 265–291. several urban ant species. J. Econ. Entomol. 95, 1222–1228. Mikheyev, A.S., Tschinkel, W.R., 2004. Nest architecture of the ant formica pallidefulva: Jílková, V., Matějíček, L., Frouz, J., 2011. Changes in the pH and other soil chemical structure, costs and rules of excavation. Insect. Soc. 51, 30–36. parameters in soil surrounding wood ant (Formica polyctena) nests. Eur. J. Soil Biol. Nelson, D.W., Sommers, L.E., 1982. Total carbon, organic carbon and organic matter. In: 47, 72–76. Page, A.L., Miller, R.H., Keeney, D.R. (Eds.), Methods of Soil Analysis. Part 2, second Johnson, R.A., 2010. Habitat segregation based on soil texture and body size in the seed- ed. Agronomy Monograph ASA and SSSA, Madison, WI, pp. 534–580. harvester ants Pogonomyrmex rugosus and P. barbatus. Ecol. Entomol. 25, 403–412. Ohashi, M., Finer, L., Domisch, T., Risch, A.C., Jurgensen, M.F., 2005. CO2 efflux from a Jones, C.G., Lawton, J.H., Shachak, M., 1994. Organisms as ecosystemengineers. Oikos red wood ant mound in a boreal forest. Agric. For. Meteorol. 130, 131–136. 69, 373–386. Quinton, J.N., Edwards, G.M., Morgan, R.P.C., 1997. The infl uence of vegetation species Jouquet, P., Janeau, J.L., Pisano, A., Hai, T.S., Orange, D., Minh, L.T.N., Valentin, C., and plant properties on runoff and soil erosion: results from a rainfall simulation 2012. Influence of earthworms and termites on runoff and erosion in a tropical steep study in south east Spain. Soil Use Manag. 13 (3), 143–148. slope fallow in Vietnam: a rainfall simulation experiment. Appl. Soil Ecol. 61, Robinson, E.J.H., Holcombe, M., Ratnieks, F.L.W., 2008. The organization of soil disposal 161–168. by ants. Anim. Behav. 75, 1389–1399. Karlen, D.L., Ditzler, C.A., Andrews, S.S., 2003. Soil quality: why and how? Geoderma Schmidt, L.K., Zimmermann, A., Elsenbeer, H., 2014. Ant mounds as a source of sediment 114, 145–156. in a tropical rainforest? Hydrol. Process. 28 (13), 4156–4160. Kilpelainen, J., Finer, L., Niemela, P., Domisch, T., Neuvonen, S., Ohashi, M., Sundstrom, Shen, H.O., Zheng, F.L., Wen, L.L., Han, Y., Hu, Wei, 2016. Impacts of rainfall intensity L., 2007. Carbon, nitrogen and phosphorus dynamics of ant mounds (Formica rufa and slope gradient on rill erosion processes at loessial hillslope. Soil Tillage Res. 155, group) in managed boreal forests of different successional stages. Appl. Soil Ecol. 36, 429–436. 156–163. Smith, C.R., Tschinkel, W.R., 2005. Object depots in the genus Pogonomyrmex: exploring LeBrun, E.G., Moffett, M., Holway, D.A., 2011. Convergent evolution of levee building the “who”, what, and where. J. Insect Behav. 18, 859–879. behavior among distantly related ant species in a floodplain ant assemblage. Insect. Tschinkel, W.R., 2003. Subterranean ant nests: trace fossils past and future? Palaeogeogr. Soc. 58, 263–269. Palaeoclimatol. Palaeoecol. 192, 321–333. Leite, P.A.M., Carvalho, M.C., Wilcox, B.P., 2018. Good ant, bad ant? Soil engineering by Wang, Y.Q., Shao, M.A., Shao, H.B., 2010. A preliminary investigation of the dynamic ants in the Brazilian Caatinga differs by species. Geoderma 323, 65–73. characteristics of dried soil layers on the Loess Plateau of China. J. Hydrol. 381, 9–17. Léonard, J., Perrier, E., Rajot, J.L., 2004. Biological macropores effect on runoff and in- Wheeler, W.M., 1907. The fungus-growing ants of North America. Bull. Am. Mus. Nat. filtration: a combined experimental and modelling approach. Agric. Ecosyst. Environ. Hist. 23, 669–807. 104, 277–285. Whitford, W.G., 2003. The functional significance of cemented nest caps of the harvester Li, S.Q., Ren, S.J., Li, S.X., 2004. Seasonal change of soil microbial biomass and the re- ant, Pogonomyrmex maricopa. J. Arid Environ. 53, 281–284. lationship between soil microbial biomass and soil moisture and temperature. Plant Yang, X., Shao, M.A., Li, T.C., Jia, Y.H., Jia, X.X., Huang, L.M., 2018. Structure char- Nutr. Fertil. Sci. 10 (1), 18–23 (in Chinese with English abstract). acteristics of Camponotus Japonicus nests in northern part of Loess Plateau and in- Li, X.R., Gao, Y.H., Su, J.Q., Jia, R.L., Zhang, Z.S., 2014. Ants mediate soil water in arid fluencing factors. Acta Pedol. Sin. 55, 868–878. desert ecosystems: mitigating rainfall interception induced by biological soil crusts? Zhang, L., Wang, J., Bai, Z., Lv, C., 2015. Effects of vegetation on runoff and soil erosion Appl. Soil Ecol. 78, 57–64. on reclaimed land in an opencast coal-mine dump in a loess area. Catena 128, 44–53. Li, T.C., Shao, M.A., Jia, Y.H., 2017a. Effects of activities of ants (Camponotus japonicus) Zhou, G., Wei, X., Yan, J., 2002. Impacts of eucalyptus (Eucalyptus exserta) plantation on on soil moisture cannot be neglected in the northern Loess Plateau. Agric. Ecosyst. sediment yield in Guangdong province, southern China—a kinetic energy approach. Environ. 239, 182–187. Catena 49, 231–251. Li, T.C., Shao, M.A., Jia, Y.H., 2017b. Characteristics of soil evaporation and temperature

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