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Article

The Impact of an Alien Snail Pomacea canaliculata Invading Coastal Saline Soils on Soil Chemical and Biological Properties

by
Qi Chen
1,2,3,4,
Yingying Zhou
1,2,3,4,
Yue Qi
1,2,3,4,
Wen Zeng
1,2,3,4,
Zhaoji Shi
1,2,3,4,
Xing Liu
1,2,3,4 and
Jiaen Zhang
1,2,3,4,*
1
Guangdong Engineering Research Center for Modern Eco-Agriculture and Circular Agriculture, Guangzhou 510642, China
2
Department of Ecology, College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China
3
Guangdong Provincial Key Laboratory of Eco-Circular Agriculture, South China Agricultural University, Guangzhou 510642, China
4
Key Laboratory of Agro-Environment in the Tropics, Ministry of Agriculture and Rural Affairs, Guangzhou 510642, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(3), 540; https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy14030540
Submission received: 27 December 2023 / Revised: 5 February 2024 / Accepted: 19 February 2024 / Published: 6 March 2024
(This article belongs to the Section Soil and Plant Nutrition)
Browse Figures
Versions Notes

Abstract

:
Recent studies have indicated that the invasive apple snail (Pomacea canaliculata) exhibits tolerance to the salinity levels present in coastal agricultural soils, suggesting that apple snails could potentially invade salt-affected coastal agricultural areas. However, the effects of the alien snail Pomacea canaliculata invasion on coastal saline soils, such as in terms of soil properties, microbial diversity, and abundance, remain poorly understood. To fill this gap, we conducted experiments involving three salinity levels (0, 2‰, and 5‰, w/w), coupled with varying snail densities (0, 5, and 10 snails per box), applied to agricultural soil. We analyzed soil chemical properties, enzyme activities, and bacterial communities. The findings revealed that heightened soil salinity increased soil electrical conductivity (EC) (exceeding 1312.67 μS cm−1). Under saline conditions, snail treatments significantly increased the soil organic matter (SOM) content from 15.82 mg kg−1 to 18.69 mg kg−1, and concurrently diminished the dissolved organic carbon (DOC) from 47.45 mg kg−1 to 34.60 mg kg−1. Both snail and salinity treatments resulted in ammonia nitrogen (NH4+-N) accumulation, while nitrate nitrogen (NO3−-N) concentrations remained low in salt-affected soils. A notable positive correlation existed between the EC and the activities of hydroxylamine reductase (HR) and peroxidase (POD), where HR exhibited a positive correlation with NH4+-N, and POD displayed a negative correlation with NO3−-N. Salinity substantially decreased the diversity and altered the composition of soil bacterial community, with the phyla Bacteroidota, Proteobacteria, and Firmicutes adapting to salt-affected soil environment and proliferating. Structural equation modeling (SEM) analysis indicated that snails exerted a direct influence on soil-available nitrogen (including NO3−-N and NH4+-N), while salinity impacted available nitrogen by modulating soil enzyme activities and bacterial communities. Our findings provide insights into how soil responds to the concurrent impacts of snail invasion and soil salinization, establishing some references for future research.

1. Introduction

The introduction of invasive species can exert profound and far-reaching effects on native ecosystems, both through direct and indirect mechanisms [1,2,3]. Pomacea canaliculata, commonly known as the apple snail, was introduced from South America to Southeast Asia in the 1980s for cultivation purposes. However, they have proliferated in farmland and wetland ecosystems, destroyed crops, caused massive losses, and eventually became global invaders, threatening agroecosystems around the globe [4,5,6,7]. Previous studies on the impact of apple snails on the environment have mainly focused on their herbivory on paddy and wetland plants [6], whereas their influences on soil properties and biological traits have remained poorly studied. Although O’Neil et al. [8] reported little effect of snails on soil properties and processes, Jong-Song et al. [9] observed that the movements of the apple snails could effectively enhance soil permeability and bulk density. Moreover, the excretions of these snails were found to contribute substantially to improvements in soil organic matter, as well as elevated levels of nitrogen, phosphorus, and potassium [9]. Additionally, Hall Jr. et al. [10] demonstrated that invasive snails (Potamopyrgus antipodarum) significantly impact nitrogen cycling in the environment, as their excretions fulfill two-thirds of the ammonia requirements of other organisms. Therefore, comprehensive research is necessary to understand invasive apple snails’ direct and indirect impacts on soil ecosystem.
The invader Pomacea canaliculata exhibits remarkable adaptability to variations in temperature, drought, and water pollution, enabling them to establish populations promptly in both natural and man-made aquatic environments [11,12,13,14,15]. Their ability to survive and reproduce in salt-affected environments is noteworthy, with studies revealing their capacity to endure stressors of 8 practical salinity units (PSU) for 25–31 days [16]. Furthermore, their eggs can survive and develop through recurring saltwater tides [17]. On the other hand, sea levels are rising due to climate change, negatively impacting coastal areas through seawater intrusion in surface and subsurface water bodies [18,19,20]. According to the latest data from the Food and Agriculture Organization of the United Nations (FAO), there were approximately 883 million hectares of saline soil worldwide, and 8.7% of the total global land area was affected by salinity in 2021. At the same time, in response to the challenges posed by population growth and food demand, coastal mudflats have become crucial for agriculture, with rice emerging as a primary crop [21,22,23]. However, in rice irrigation, maintaining salt content below 2.0 g L−1 is essential for optimal rice growth, aligning with the tolerance range of the apple snail [24]. Moreover, it is crucial to note that apple snails have been found in saltwater lakes, coastal areas, and brackish water ecosystems [25,26,27], indicating that apple snails are invading the coastal areas. All of the above evidence points to the potential risk of apple snails invading coastal farmland.
Elevated salinity in an environment leads to diminished concentrations of nutrient-related parameters, decreased microbial diversity, and substantial shifts in taxonomic structure [28,29], including inhibiting soil bacterial communities responsible for mediating nitrogen cycling [30]. Notably, some reports have highlighted that the invasion of the apple snail contributes to the remediation of salt-affected soils [9,31,32]. The main mechanism is that the decomposition of snail shells elevates calcium ions and reduces the sodium adsorption rate (SAR). However, there are still few studies on the effects of an apple snail invasion and salt invasion on soil properties, especially on the combined effects on soil physicochemical properties and microbial communities. Thus, our study aimed to (1) investigate changes in soil properties and bacterial communities in response to soil salinization and apple snail invasion; (2) assess the effects on nutrient availability when agricultural land is exposed to both salinization and apple snail invasion; and (3) elucidate whether a synergistic effect exists between apple snail invasion and soil salinization. Our experiments are aim to answer these questions, provide critical insights into the changes in soil properties and microbial communities under the dual influence of apple snail invasion and soil salinization, and lay the groundwork for understanding apple snail invasions in coastal areas.

2. Materials and Methods

2.1. Snail Maintenance and Soil Preparation

In August 2022, snails and soil were gathered for the experiment at the teaching and research farm of South China Agricultural University in Guangdong (113°21′ E, 23°9′ N), China. The sampling site had a subtropical monsoon climate, with a mean annual temperature (MAT) of 23.2 °C and a mean annual precipitation (MAP) of 1891.9 mm, respectively. Apple snails were collected from paddy field. The pH of the water in the paddy field was 6.45 ± 0.05, while the salinity was 0.01 ± 0.00 ppt (part per thousand). Mature apple snails [33] (shell lengths = 28.32 ± 0.56 mm) were selected for the study and kept under a controlled photoperiod of 12L: 12D and a temperature of 28 ± 2 °C for two weeks before testing.
Soil samples were gathered from the top 20 cm of the rice field. The soil texture was sand clay, consisting of sand (57.56%), silt (6.13%), and clay (36.31%), belonging the Ultisols group according to the USDA taxonomy [34]. Then, the collected soil was naturally dried and sieved with a 2 mm mesh. The principal properties of the soil pH (extracted using H2O), electrical conductivity (EC), contents of total nitrogen (TN), nitrate nitrogen (NO3−-N), ammonium nitrogen (NH4+-N), and soil organic matter (SOM) were 6.20, 65.00 μS cm−1, 1.427 g kg−1, 4.508 mg kg−1, 13.601 mg kg−1, and 25.210 g kg−1, respectively.

2.2. Experimental Treatments

In August 2022, we placed 3.5 kg of soil in a plastic box (29.3 × 19.8 × 14.5 cm) to a depth of 5 cm and added 1 L of aerated tap water. There were 25 holes, each with a diameter of 0.5 cm, punched into the lid of each box to enable adequate ventilation. Simultaneously, in referring to the method of Zhen et al. [23], sea salt was incorporated into the boxes at three concentrations, determined based on the soil dry weight (w/w): (1) N (no salt addition); (2) L (low salinity, 2 g kg−1, 2‰); and (3) H (high salinity, 5 g kg−1, 5‰). The sea salt was composed of NaCl (68.88%), NaHCO3 (12.75%), MgCl2 (8.67%), MgSO4 (5.36%), CaCl2 (2.55%), and KCl (1.79%). Afterward, the treatment boxes were kept for a week to stabilize the physicochemical properties of the soil. Each salinity treatment had three P. canaliculata snail addition treatments: (1) no snail; (2) five snails per box; and (3) ten snails per box. The current study involved a total of nine treatments (N0, N5, N10, L0, L5, L10, H0, H5, H10). Each treatment was replicated three times (N = 3) (Figure 1). The number of snails was selected based on the optimal growth density of golden apple snails, which has also been a commonly used density in experiments [33]. The salinity levels mentioned above relied upon the environmental conditions previously documented in paddy soils [32], the tolerance of snails to salinity [35], and soil response to changes in salinity [28]. A salinity concentration of 2‰ was utilized in this research to mimic the present salinity levels of the soil, whereas a salinity concentration of 5‰ was selected to investigate the probable impacts of future increases in soil salinity. Throughout the 42-day experimental duration, a consistent temperature of 28 °C was maintained in the experimental environment. During the experiment’s duration, the snails’ survival was monitored daily, and they were not provided with any food. Snails were considered dead when unresponsive to operculum stimulation with a dissecting needle [36]. If a snail was found dead, it was immediately replaced with a snail of equal size.

2.3. Soil Sampling

At the end of the experiment, soil samples were collected, passed over a 2 mm sieve, and divided into three parts. The first sub-sample was left to air dry and then used to measure the soil pH, electrical conductivity, contents of total nitrogen and soil organic matter, and the activities of the enzymes. The next sub-sample was refrigerated at 4 °C until it was analyzed for contents of ammonium nitrogen (NH4+-N), nitrate nitrogen (NO3−-N), microbial biomass carbon (MBC), microbial biomass nitrogen (MBN), and dissolved organic carbon (DOC). The last sub-sample was frozen at −80 °C for the extraction of total genomic DNA.

2.4. Analyses of Soil Characteristics and Microbial Biomass

A portable pH meter (Seven2Go, Mettler-Toledo Instruments, Shanghai, China) and EC meter (DDS-307, INASE Scientific Instrument, Shanghai, China) were used to measure the pH and electrical conductivity (EC) of the soil suspension (at a 1:5 water ratio), respectively [37]. The total nitrogen content was measured using an elemental analyzer (Analyzer Vario MICRO) manufactured by Elementar in Germany [38]. The soil organic carbon (SOC) content was determined using the potassium dichromate oxidation method. The SOC content was multiplied by an empirical coefficient (1.724) to obtain the content of soil organic matter (SOM) [39]. Extracted with 2 M KCl, the NO3−-N and NH4+-N contents were determined with a colorimetric technique in an AutoAnalyser III continuous Flow Analyzer (Bran + Luebbe, German) [38]. The MBC and MBN contents were extracted via chloroform fumigation and then analyzed using a TOC analyzer (Multi C/N 3000, Analytik Jena, Germany) [40]. The DOC was extracted with 0.5 M K2SO4 and then analyzed with a Vario TOC elemental analyzer (Elementar, Hanau, Germany).

2.5. Analysis of Soil Enzyme Activities

In this study, the activities of peroxidase (POD), phenol oxidase (PO), β-glucosidase (BG), hydroxylamine reductase (HR), and cellobiohydrolase (CBH) of the soil were analyzed. POD activity was measured photometrically using a L-3,4-dihydroxyphenylalanine (DOPA) substrate [41]. PO activity was quantified via spectrophotometry, utilizing L-3,4-dihydroxyphenylalanine as the substrate [42]. The activity of BG was measured using the procedure of Marx et al. [43]. The soil HR activity was detected with a detection kit from Mofan Biotech in Nanjing, China. The assay of CBH was conducted with the Cellulase Assay Kit from Solarbio in Beijing, China.

2.6. Analysis of Soil Bacterial Community

Soil DNA was obtained with the PowerSoil DNA Isolation Kit (MoBio Laboratories, Carlsbad, CA, USA). A 1% agarose gel and Thermo Scientific NanoDrop spectrophotometer were used to assess the quality of genomic DNA. The V3-4 region of the 16S rRNA gene was amplified with forward 338F (5′-ACTCCTACGGAGGCAGCAG-3′) and reverse 806R (5′-GGACTACNNGGGGTATCTAAT-3′) primer sequences [44]. Each primer was appended with an 8-bit barcode sequence at the 5′ end, respectively, provided by Allwegene, Beijing, China.
PCR reactions were carried out in 25 μL reaction volumes on a Mastercycler Gradient (Eppendorf, Germany). The composition included 12.5 μL of 2× Taq PCR MasterMix, 3 μL of BSA at a concentration of 2 ng/μL, 1 μL of Forward Primer at 5 μM, 1 μL of Reverse Primer at 5 μM, 2 μL of template DNA, and 5.5 μL of ddH2O. PCR conditions included 95 °C for 5 min and 28 cycles of 95 °C for 45 s, 55 °C for 50 s and 72 °C for 45 s with a final extension at 72 °C for 10 min. After that, the PCR products were purified, and deep sequencing was performed on the Miseq platform at the Allwegene Company in Beijing. After the run, we used Illumina Analysis Pipeline Version 2.6 to analyze images, call bases, and estimate errors. A thorough screening of the raw data entailed excluding sequences shorter than 230 base pairs, those with a low-quality score (≤20), those containing ambiguous bases, and those not precisely matching primer sequences and barcode tags. Additionally, sequences were sorted based on sample-specific barcode sequences. Reads with 97% similarity were clustered into operational classification units (OTUs) [45], and different taxonomic groups were classified based on the SILVA128 database [46] using the Ribosomal Database Project (RDP) classifier.

2.7. Data Analysis

The data were obtained from three different tests, and the average with standard deviation was calculated. The analysis of the data was carried out in R (v4.3.1) software. The influences of the treatments on soil properties, microbial biomass, and the activities of enzymes were determined through a two-way analysis of variance. In addition, the analysis was carried out using either Duncan’s test for one-way ANOVA or Fisher’s least significant difference (LSD) for multiple comparisons. The significance level was set at p < 0.05. We used the OTU information to analyze the richness and diversity indices and plotted a bar chart based on the results of the taxonomic annotation and the relative abundance. Linear regression analysis was used to reveal the relationship between soil electrical conductivity and bacterial alpha diversity (Chao1 and Shannon index). The OTU information was analyzed using Cluster Analysis and Principal Coordinate Analysis (PCoA) [47]. Redundancy data analysis (RDA) was used to investigate the associations between soil characteristics and soil enzyme activities, as well as between soil characteristics and bacterial phyla. Pearson’s analysis was applied to study the relationship among the soil characteristics, the microbial biomass, the enzyme activities, and the bacterial communities. A structural equation modeling (SEM) analysis was carried out with SPSS Amos 24.0 to evaluate the effects of the snails and the salinity, represented by the conductivity of the soil, on the available nitrogen. Before SEM, principal component analysis (PCA) was performed for dimensionality reduction [48]. Available nitrogen referred to the first axis of PCA analysis (explained 60.62%) for NH4+-N and NO3−-N. The key factors were SOM, MBN, bacterial diversity (Shannon index), and enzyme activities (the first axis of PCA analysis for five soil enzyme activities, CBH, BG, PO, POD, and HR, which explained 64.18%). For models to have a satisfactory fit, the degree of freedom-normalized chi-square (χ2/df) should have been less than 3, and the goodness-of-fit index (GFI) should have been greater than 0.9 [49].

3. Results

3.1. Soil Properties and Microbiological Activity

The variations in soil chemical properties and microbial biomass based on the specific salt-affected environment, as well as the addition of snails, are depicted in Figure 2. Except for the addition of five snails, the highest salinity treatment significantly increased pH (p < 0.05, Figure 2a). Salinity treatment significantly enhanced the soil electrical conductivity (EC) (p < 0.05, Figure 2b). The NO3−-N content in the salt treatment remained at a low level (Figure 2d). The addition of ten snails and a higher salinity significantly raised the NH4+-N content in the salt-affected soil (p < 0.05, Figure 2e). In contrast, ten snail addition and a higher salinity reduced the MBN content in the salt-affected soil (p < 0.05, Figure 2f). In addition, under salinity stress conditions, the introduction of snails significantly decreased the DOC content, while the SOM showed a contrasting trend (p < 0.05, Figure 2g,h). Low salinity stress significantly increased the soil microbial biomass carbon (MBC) content (p < 0.05, Figure 2i).
Two-way ANOVA showed that salinity significantly affected the soil chemical properties (p < 0.05). The contents of NO3−-N, NH4+-N, MBN, and SOM were significantly influenced by the effects of salinity, snail addition, and their interaction (p < 0.05, Figure 2d–f,h).

3.2. Soil Enzyme Activities

Soil enzyme activity was affected by the salinity and snail treatments (Figure 3). Salinity caused a substantial rise in POD activity (p < 0.05, Figure 3b). Low salinity significantly increased BG and CBH activity (p < 0.05, Figure 3d,e). One-way ANOVA showed that snail treatments significantly affected HR and POD activities (p < 0.05, Figure 3a,b). Under high-salinity conditions, the presence of snails led to an increase in the activities of soil enzymes BG and CBH (Figure 3d,e). What’s more, there was a significant interaction effect between salinity and snails on the soil HR, POD, PO, and BG activities (p < 0.05, Figure 3a–d).

3.3. Soil Bacterial Community

Snails and salinity altered the alpha diversity (Chao1 and Shannon index) of the soil’s bacterial community (Figure 4a,b). The high salinity treatment exhibited the low Chao1 index and significantly reduced the Shannon index (p < 0.05). The soil bacterial communities were dominated by Bacteroidota, Nitrospirota, Proteobacteria, and Acidobacteriota (Figure 4c). Compared with the other salinity treatments, high-salt treatments had the highest relative abundance of Proteobacteria (17.92–19.48%) and Firmicutes (11.53–12.97%).
The PCoA on the OTU level showed that salinity treatment significantly altered the soil bacterial community structure (Figure 4d, p = 0.001). Linear regression analysis showed that the alpha diversity (Chao1 and Shannon index) of the bacterial community decreased with increasing EC (Figure 4e,f, p < 0.001). However, the bacterial community in the snail-added soil did not differ significantly from those in the control soil.

3.4. Relationships among Soil Properties, Enzyme Activities, and Bacterial Phyla

An RDA analysis indicated that 79.52% of the variance in soil properties was explained by the enzyme activities (Figure 5a). This analysis revealed that all enzyme activities were significantly associated with soil properties (Figure 5a and Table 1, p < 0.05). Similarly, the changes in the soil bacterial community composition were reflected in the first two axes explaining 67.32% of the variance (Figure 5b). It was revealed that the pH value and the contents of NH4+-N, NO3−-N, SOM, and TN were significantly associated with the soil bacterial community composition (Figure 5b and Table 1, p < 0.01).
The correlation analysis indicated that there was a significantly positive correlation between soil EC and the soil pH, SOM, DOC and TN contents, and HR and POD activities, while there was a significantly negative correlation with the Shannon index, Chao1 index, and NO3−-N content (Figure 5c, p < 0.05). Soil MBC and MBN were significantly and positively correlated with soil enzyme activities except HR (p < 0.05). Both NO3−-N and NH4+-N contents were significantly negatively correlated with the MBC and MBN contents and activities of CBH, PO, and BG (p < 0.05). Furthermore, the correlation between the soil properties and relative abundance of the top 10 bacterial phyla was also investigated (Figure 5d). The abundances of the dominant phyla Proteobacteria, Firmicutes, and Bacteroidota were positively correlated with the EC (p < 0.05), while those of Nitrospirota, Sva0485, Myxococcota, Chloroflexi, and Acidobacteriota were negatively correlated with the EC (p < 0.05). The NH4+-N content had a significantly positive correlation with the Firmicutes and Bacteroidota abundances, and the NO3−-N content had a significantly positive correlation with the Nitrospirota abundance (p < 0.05).
The structural equation model (SEM) demonstrated that apple snails had a direct effect on the available nitrogen in the soil. In contrast, soil salinity had an indirect effect on the available nitrogen through changes in bacterial diversity, enzyme activity, microbial biomass nitrogen, and soil organic matter (Figure 6). In total, soil electrical conductivity had a standardized total path coefficient of 0.058, whereas snails showed a standardized total path coefficient of 0.181.

4. Discussion

4.1. Effects of Snail and Salinity on Soil Properties and Microbiological Biomasses

This study found that soil chemical properties and microbial biomasses varied with the salt-affected environment and snail addition (Figure 2). First, salinity increased the soil EC, and high salinity held a high level of pH (Figure 2a,b). This may be due to increases in basic cations (K+, Ca2+, Mg2+, and Na+). The addition of salt increased the K+, Ca2+, Mg2+, and Na+ ions, and they exchanged with Al3+, Fe2+, and Mn2+ ions at the soil adsorption sites [50]. This reaction hinders the hydrolysis produced by the Al3+, Fe2+, and Mn2+ ions, resulting in a decrease in the production of H+ ions and hence an increase in soil pH. This result indicates that in coastal farmlands, seawater intrusion would lead to soil salinization and soil alkalinization [51], threatening crop growth. Furthermore, it was noted that an increase in calcium carbonate content in the soil would lead to an increase in pH [52], but in our study, snail addition (with shells primarily composed of calcium carbonate) did not have an effect on soil pH. However, the addition of snails increased the soil EC; this may be due to the increase in soil calcium ion content caused by the snail shells [31]. Jong-Song and Song-Ho [31] showed that calcium ions decreased the soil sodium adsorption rate (SAR), suggesting the potential role of snail additions in reducing the salinity effect on crops [53].
Second, our study revealed significant impacts of both salinity treatment and snail presence on various nitrogen forms, including TN, NH4+-N, NO3−-N, and MBN. In no-saline conditions, snails enhanced the TN content (Figure 2c), which is likely attributed to their nitrogen-rich excrement [32]. In salt-affected soils, the introduction of snails increased the NH4+-N levels, aligning with the findings of Hall Jr et al. [10] on the contribution of invasive snails (Potamopyrgus antipodarum) to ammonium regeneration. This effect may result from snails adapting their respiratory metabolism to maintain osmotic pressure balance under salinity stress, thus leading to increased oxygen consumption and ammonia excretion rates [54]. Similarly, compared with the low-salinity treatment, the high-salinity soil also showed an increase in NH4+-N (Figure 2e). In contrast, nitrate nitrogen (NO3−-N) remained at low concentrations in salt-affected soil (Figure 2d). These effects may stem from a diminished abundance of key nitrogen cycle function genes, which inhibit ammonia oxidation and nitrite oxidation [55]. This inhibition results in the accumulation of NH4+-N and the reduction of NO3−-N at higher salinity levels [30]. Zhen Zhen et al. [23] proposed that cultivating rice in saline soil in coastal areas could alleviate the inhibitory effect of salt on nitrogen cycling genes, as rice cultivation led to an increase in the amoA genes of ammonia-oxidizing archaea (AOA) and ammonia-oxidizing bacteria (AOB). Furthermore, the addition of snails tended to reduce soil MBN in salt-affected soil (Figure 2f). This reduction could be attributed to snails potentially accelerating nitrogen mineralization, leading to a decrease in soil microbial biomass nitrogen [8].
Third, our study also paid attention to the changes in carbon, including SOM, DOC, and MBC. In saline conditions, snails significantly increased the SOM content and decreased the DOC content, altering the trends of the salinity effect. This shift can be explained by the accumulation of snail excreta and their movement. Recent research suggests that snails excrete approximately 10% of their body weight in waste matter daily and that their excrement contains an amount of organic matter (11.75%) [32]. The sustained buildup of apple snail waste enriches soil horizons and increases the soil SOM [56]. This finding aligns with the work of Jong-Song et al. [9], who highlighted the beneficial impact of apple snails on reclaimed sodic soil with low salt concentrations over six years. Jong-Song et al.’s study demonstrated that snails increase soil organic matter and elevate nitrogen, phosphorus, and potassium levels in the soil [9]. These results prompt us to consider the potential of apple snails in improving coastal saline soils.

4.2. Effects of Snail and Salinity on Soil Enzyme Activities

By altering the osmotic pressure and ion effects, salinity could influence microbial community composition and soil enzyme activities [57]. Despite previous reports indicating a negative impact of salinity on enzymes [58,59], our research demonstrated increased activities of HR and POD under salinity conditions. Moreover, in a low-salinity environment (2‰, w/w), PO, BG, and CBH exhibited high activities. This positive correlation between soil enzyme activities and salinity aligns with Yang et al.’s findings [60], who suggested that salinity stress can enhance the activity of stress-resistant enzymes. The heightened enzyme activity observed in our study could be attributed to bacterial community changes, which could produce enzymes with antistress and growth-promoting functions. For instance, phenol oxidase (POD) and peroxidase (PO) could be used for various purposes, including ontogeny, defense, and acquiring carbon and nitrogen [61]. At lower salinities suitable for survival, microorganisms would produce these enzymes to adapt to challenging environments. Morrissey et al. [62] similarly reported a positive effect of salinity on CBH, BG, and PO activities. This increased activity was attributed to the heightened ionic strength, which affected molecular stability and the sorption of organic enzyme substrates. In salt-affected soils, increased ionic strength could break down soil microaggregates [63] and reduce the adsorption of organic compounds [64,65], increasing the solute concentration and enhancing enzymatic reaction rates. It is crucial to note that different salinity scales and experiment durations can yield varied results. While studies on hypersaline conditions and long-term exposures have suggested low enzyme activity in salt-affected soils [58,66], these aspects are beyond the scope of our study.
It was noteworthy that snails increased soil BG and CBH activities under high-salinity conditions (Figure 3d,e). This may be related to the increase in SOM produced by snails (Figure 2h). The activity of carbon-degrading enzymes, such as BG and CBH, has been found to be directly related to SOM content [67].

4.3. Effects of Snail and Salinity on Soil Bacterial Communities

From the PCoA analyses in this experiment, it was evident that soil salinity significantly influenced the bacterial community, whereas snail addition had minimal impact (Figure 4d). Salinity has been identified as a crucial regulator of soil microbe activity and global microbial distribution patterns [68,69]. In our work, salinity and soil EC primarily affected the bacterial diversity (Figure 4a,b,e,f). Consistent with prior research, higher salinity negatively impacted soil microbial activity [55,70,71]. Rath et al. [29] also observed a decrease in bacterial diversity as salinity increased in lake sediment. High salinity could increase extracellular osmotic pressure, which would cause low saline-resistant microorganisms to die [72,73,74,75]. Species with a higher salinity tolerance may gain competitive advantages and displace those with a lower salinity tolerance [75], thus becoming predominant inhabitants in salt-affected environments.
In our study, salinity had a notable impact on the composition of the bacterial community (Figure 4c,d). The dominant bacterial phyla observed mostly align with findings in salt-affected soils, where 90% of bacterial sequences belonged to six phyla (Proteobacteria, Actinobacteria, Firmicutes, Acidobacteria, Bacteroidota, and Chloroflexi) [76]. Moreover, the other two dominant phyla Nitrospirota and Desulfobacterota were found in the present experiment. Among the bacterial phyla, Bacteroidota exhibited the highest relative abundance in our high-salinity treatments, which was high-salinity-tolerant and common in brackish water and freshwater sediments [77]. Bacteroidota demonstrated the ability to utilize substrates in salt-affected soils [78,79]. In addition, the increases in Proteobacteria and Firmicutes in high-salinity treatments matched the observations of Chen et al. in a salinity test environment, where they comprised over 90% of the total relative abundances in all samples [80]. In high-salinity environments, Gamma-proteobacteria could thrive by utilizing various organic substances for energy generation [81,82]. It was also found that high salinity increased the relative abundance of Firmicutes in coastal estuarine wetlands [83]. This evidence confirmed the salinity resistances of the phyla Bacteroidota, Proteobacteria, and Firmicutes.

4.4. Interconnections among the Tested Parameters

Based on the RDA analysis, enzyme activity played a crucial role in determining soil quality (Figure 5a). Our correlation analysis underscored the clear negative relationship between soil carbon-degrading enzyme activities, such as CBH, PO, and BG, and the contents of NH4+-N and NO3−-N (Figure 5c). This is probably due to the large production of nitrogen and energy-intensive enzymes. The microbial requirements and the availability of C and N determine the production and activity of the enzymes [84]. When nutrients are in short supply, microbes will sacrifice growth and metabolism in favor of enzyme production. During this production process, the amount of nitrogen decreases. In this work, microbes responded to salinity stress by producing N-rich enzymes, resulting in a nitrogen decrease. Conversely, both MBC and MBN were positively correlated with BG, CBH, POD, and PO activities (Figure 5c, p < 0.05). MBC and MBN are organic substrates for soil enzyme reactions [85,86], and their increases enhance enzyme activities.
Nitrogen (N) is a crucial nutrient limiting crop growth and yields in coastal regions. To achieve high crop yields, the use of mineral nitrogen fertilizers in coastal areas has been steadily increasing, leading to significant ecological and environmental issues, including a low efficiency of nutrient utilization, heightened nitrogen loss, and increased greenhouse gas emissions [23]. Soil microorganisms are pivotal in assessing soil health within agricultural ecosystems, actively driving the soil nitrogen cycle [87]. Therefore, investigating the changes in microbial community structures and their relationships with nitrogen cycling in saline-affected soils holds considerable significance. In our study, TN, NH4+-N, and NO3−-N contents displayed strong associations with soil bacterial communities (Figure 5b; Table 1). A nitrogen supply is essential for microbes to adapt to salinity [88]. The abundances of phyla Firmicutes and Bacteroidota were significantly positively correlated with the NH4+-N content, and Nitrospirota with NO3−-N content (Figure 5d). These bacteria play important roles in nitrogen turnover [89,90]. Bacteroidota is involved in ammonization [91], Nitrospirota in nitrification [92], and Firmicutes in denitrification and dissimilatory nitrate reduction to ammonia [93]. Due to their high abundance and potentially important role in N cycling, the phyla Firmicutes and Bacteroidota merit further attention as biomarkers for ecosystems under salinity stress.
The structural equation model (SEM) indicated that soil salinity content (represented by the soil EC) positively influenced the soil available nitrogen (including NO3−-N and NH4+-N), but its effect was weaker than the introduction of apple snails. This result is likely due to the different effects of soil salinity on ammonia- and nitrate-nitrogen. According to the correlation analysis, the soil EC was positively correlated with ammonia nitrogen and negatively with nitrate nitrogen, which was also confirmed by Zhou et al. [94]. Overall, a higher soil salinity reduced bacterial diversity and increased enzyme activities and soil organic matter accumulation, while enzyme generation and microbial biomass nitrogen composition reduced the available nitrogen content. On the other hand, the snail treatment had a direct and considerable impact on the available nitrogen in the soil due to increased ammonia emissions through respiratory metabolism [54]. O’Neil et al. [8] also confirmed and reported that snails accelerate nitrogen mineralization.

5. Conclusions

The present study investigated the effects of soil salinity and the addition of apple snails on soil nutrients and bacterial communities. Salinity and snails increased the soil’s available nitrogen through different approaches. Increased salinity was found to elevate ammonia nitrogen content and decrease nitrate nitrogen content, while snail introduction directly led to higher ammonia nitrogen content. Specifically, salinity stimulated enzyme activity, influencing the ammonia- and nitrate-nitrogen levels. Furthermore, salinity had a detrimental effect on the bacterial community, but some salinity-tolerant bacteria such as Bacteroidota, Proteobacteria, and Firmicutes still thrived and influenced soil nitrogen availability. Although snails did not significantly impact bacterial communities and enzyme activities, their excretion and metabolism led to heightened soil organic matter and ammonium nitrogen in saline soil.
In summary, our findings provide an evidence for the effects of snails and salinity on soil’s available nitrogen and enhance our understanding of how soil properties respond to salinization and biological invasion. Despite the potential risk of apple snail invasions into coastal saline farmland, our experiment suggests potential benefits, such as increased soil organic matter and available nitrogen. Nevertheless, it should be noted that the damage to crops caused by apple snails is undeniable. Future studies should explore the impact of apple snail invasions on coastal agricultural activities to guide production.

Author Contributions

Conceptualization, Q.C. and J.Z.; data curation, Q.C.; formal analysis, Y.Q. and W.Z.; funding acquisition, J.Z.; investigation, Y.Z., Y.Q. and W.Z.; methodology, Q.C., Z.S. and X.L.; project administration, J.Z.; resources, Y.Z., Y.Q., W.Z. and J.Z.; software, Z.S. and X.L.; supervision, J.Z.; validation, X.L.; visualization, Y.Z.; writing—original draft, Q.C.; writing—review and editing, Q.C. and J.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China (grant numbers 31870525, 31770484, 41871034, and 31901229) and the Guangdong Science and Technology Project (grant number 2019B030301007).

Data Availability Statement

The data presented in this study are available in the article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Pictures of the experimental setup (a) and the snails (b).
Figure 1. Pictures of the experimental setup (a) and the snails (b).
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Figure 2. Effects of different treatments on soil chemical properties and microbial biomasses (carbon and nitrogen) under the different salinities of soil and the snail-introduction treatments. The properties include pH (a), EC (b), TN (c), NO3−-N (d), NH4+-N (e), MBN (f), DOC (g), SOM (h), and MBC (i). The plots are labeled no snail added (CK), five snails added (Five), and ten snails added (Ten). The horizontal coordinates N, L, and H refer to the non-salted soil (N), low-salinity soil (L), and high-salinity soil (H) treatments, respectively. Data are shown as mean ± standard error (N = 3). The different lowercase and uppercase letters denote the significant differences (p < 0.05) across snail and salinity treatments, respectively. Asterisks denote significant differences in two-way ANOVA (NS p ≥ 0.05, ** p < 0.01, *** p < 0.001).
Figure 2. Effects of different treatments on soil chemical properties and microbial biomasses (carbon and nitrogen) under the different salinities of soil and the snail-introduction treatments. The properties include pH (a), EC (b), TN (c), NO3−-N (d), NH4+-N (e), MBN (f), DOC (g), SOM (h), and MBC (i). The plots are labeled no snail added (CK), five snails added (Five), and ten snails added (Ten). The horizontal coordinates N, L, and H refer to the non-salted soil (N), low-salinity soil (L), and high-salinity soil (H) treatments, respectively. Data are shown as mean ± standard error (N = 3). The different lowercase and uppercase letters denote the significant differences (p < 0.05) across snail and salinity treatments, respectively. Asterisks denote significant differences in two-way ANOVA (NS p ≥ 0.05, ** p < 0.01, *** p < 0.001).
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Figure 3. Effects of different treatments on soil enzyme activities under the different salinity soils and the snail-introduction treatments. The enzyme activities include HR (a), POD (b), PO (c), BG (d), and CBH (e). The plots are labeled as no snail added (CK), five snails added (Five), and ten snails added (Ten). The horizontal coordinates N, L, and H refer to the non-salted soil (N), low-salinity soil (L), and high-salinity soil (H) treatments, respectively. Data are shown as mean ± standard error (N = 3). The different lowercase and uppercase letters denote the significant differences (p < 0.05) across snail and salinity treatments, respectively. Asterisks denote significant differences in two-way ANOVA (NS p ≥ 0.05, ** p < 0.01, *** p < 0.001).
Figure 3. Effects of different treatments on soil enzyme activities under the different salinity soils and the snail-introduction treatments. The enzyme activities include HR (a), POD (b), PO (c), BG (d), and CBH (e). The plots are labeled as no snail added (CK), five snails added (Five), and ten snails added (Ten). The horizontal coordinates N, L, and H refer to the non-salted soil (N), low-salinity soil (L), and high-salinity soil (H) treatments, respectively. Data are shown as mean ± standard error (N = 3). The different lowercase and uppercase letters denote the significant differences (p < 0.05) across snail and salinity treatments, respectively. Asterisks denote significant differences in two-way ANOVA (NS p ≥ 0.05, ** p < 0.01, *** p < 0.001).
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Figure 4. The diversity and composition of the bacterial community and its relationship with soil EC under the different salinities of soils and the snail-introduction treatments. (a) Chao1 index and (b) Shannon index of bacterial community. The different lowercase and uppercase letters denote the significant differences (p < 0.05) across snail and salinity treatments, respectively. (c) Relative abundance of the top 10 bacterial phyla. (d) PCoA plot of bacterial community structure. (e) Trends in the bacterial richness (Chao1) of the bacterial community with EC. (f) Trends in the bacterial diversity (Shannon) of the bacterial community with EC.
Figure 4. The diversity and composition of the bacterial community and its relationship with soil EC under the different salinities of soils and the snail-introduction treatments. (a) Chao1 index and (b) Shannon index of bacterial community. The different lowercase and uppercase letters denote the significant differences (p < 0.05) across snail and salinity treatments, respectively. (c) Relative abundance of the top 10 bacterial phyla. (d) PCoA plot of bacterial community structure. (e) Trends in the bacterial richness (Chao1) of the bacterial community with EC. (f) Trends in the bacterial diversity (Shannon) of the bacterial community with EC.
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Figure 5. Relationships among soil properties, enzyme activities, and bacterial community under the different salinity soils and the snail-introduction treatments. (a) Redundancy analysis (RDA) between soil properties and enzyme activities. (b) Redundancy analysis (RDA) between soil properties and bacterial phyla. (c) Pearson correlation among soil properties and enzyme activities. * p < 0.05, ** p < 0.01, *** p < 0.001. (d) Pearson correlation between soil properties and the relative abundance of the top 10 bacterial phyla. * p < 0.05. Abbreviations: EC, electrical conductivity; SOM, soil organic matter; DOC, dissolved organic carbon; TN, total nitrogen; NH4+-N, ammonium nitrogen; NO3−-N, nitrate nitrogen; MBC, microbial biomass nitrogen; MBN, microbial biomass nitrogen; BG, β-glucosidase; CBH, cellobiohydrolase; HR, hydroxylamine reductase; PO, phenol oxidase; POD, peroxidase.
Figure 5. Relationships among soil properties, enzyme activities, and bacterial community under the different salinity soils and the snail-introduction treatments. (a) Redundancy analysis (RDA) between soil properties and enzyme activities. (b) Redundancy analysis (RDA) between soil properties and bacterial phyla. (c) Pearson correlation among soil properties and enzyme activities. * p < 0.05, ** p < 0.01, *** p < 0.001. (d) Pearson correlation between soil properties and the relative abundance of the top 10 bacterial phyla. * p < 0.05. Abbreviations: EC, electrical conductivity; SOM, soil organic matter; DOC, dissolved organic carbon; TN, total nitrogen; NH4+-N, ammonium nitrogen; NO3−-N, nitrate nitrogen; MBC, microbial biomass nitrogen; MBN, microbial biomass nitrogen; BG, β-glucosidase; CBH, cellobiohydrolase; HR, hydroxylamine reductase; PO, phenol oxidase; POD, peroxidase.
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Figure 6. Structure equation model (SEM) for the effects of snail and soil electrical conductivity under the different salinity soils on soil biochemical factors. Blue and red arrows represent significant positive and negative correlations, and solid and dashed lines indicate significant and nonsignificant relationships (p < 0.05). EC, soil electrical conductivity; SOM, soil organic matter; MBN, microbial biomass nitrogen; Bacterial Diversity, Shannon index; Enzyme Activity (the first axis of PCA analysis for five soil enzyme activities, which explained 64.18%); available nitrogen (the first axis of PCA analysis for NH4+-N and NO3−-N, which explained 60.62%). Significance levels are indicated by * (p < 0.05), ** (p < 0.01), and *** (p < 0.001). R2 indicates the proportion of variance explained by the SEM.
Figure 6. Structure equation model (SEM) for the effects of snail and soil electrical conductivity under the different salinity soils on soil biochemical factors. Blue and red arrows represent significant positive and negative correlations, and solid and dashed lines indicate significant and nonsignificant relationships (p < 0.05). EC, soil electrical conductivity; SOM, soil organic matter; MBN, microbial biomass nitrogen; Bacterial Diversity, Shannon index; Enzyme Activity (the first axis of PCA analysis for five soil enzyme activities, which explained 64.18%); available nitrogen (the first axis of PCA analysis for NH4+-N and NO3−-N, which explained 60.62%). Significance levels are indicated by * (p < 0.05), ** (p < 0.01), and *** (p < 0.001). R2 indicates the proportion of variance explained by the SEM.
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Table 1. Statistical results of redundancy analysis (RDA) between soil properties and enzyme activity, and between bacterial phyla and soil properties.
Table 1. Statistical results of redundancy analysis (RDA) between soil properties and enzyme activity, and between bacterial phyla and soil properties.
Soil PropertiesBacterial Phyla
Explanatory VariablesVarianceFp-ValueExplanatory VariablesVarianceFp-Value
HR3.8945.41***NH4+-N2.4215.61***
BG1.00 11.64**NO3−-N1.097.04**
CBH0.779.02*pH1.006.43**
PO0.424.85*SOM1.076.90***
POD1.3313.23**TN0.734.69**
HR0.503.25*
Abbreviations: BG, β-glucosidase; CBH, cellobiohydrolase; HR, hydroxylamine reductase; PO, phenol oxidase; POD, peroxidase; NH4+-N, ammonium nitrogen; NO3−-N, nitrate nitrogen; SOM, soil organic matter; TN, total nitrogen. * p < 0.05, ** p < 0.01, *** p < 0.001.
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Chen, Q.; Zhou, Y.; Qi, Y.; Zeng, W.; Shi, Z.; Liu, X.; Zhang, J. The Impact of an Alien Snail Pomacea canaliculata Invading Coastal Saline Soils on Soil Chemical and Biological Properties. Agronomy 2024, 14, 540. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy14030540

AMA Style

Chen Q, Zhou Y, Qi Y, Zeng W, Shi Z, Liu X, Zhang J. The Impact of an Alien Snail Pomacea canaliculata Invading Coastal Saline Soils on Soil Chemical and Biological Properties. Agronomy. 2024; 14(3):540. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy14030540

Chicago/Turabian Style

Chen, Qi, Yingying Zhou, Yue Qi, Wen Zeng, Zhaoji Shi, Xing Liu, and Jiaen Zhang. 2024. "The Impact of an Alien Snail Pomacea canaliculata Invading Coastal Saline Soils on Soil Chemical and Biological Properties" Agronomy 14, no. 3: 540. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy14030540

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