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Using golden apple snail to mitigate its invasion and improve soil quality: a biocontrol approach

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Abstract

The invasive and widespread golden apple snail (GAS, Pomacea canaliculata) is a harmful crop pest in many parts of Asia. The heavy use of molluscicides to control GAS could result in soil and water pollution as well as in loss of biodiversity. A sustainable and pollution-free control method is urgently needed to counteract this invasion. In this study, we proposed using dried and powdered GAS residue to neutralize and fertilize soils. We compared the effects of adding GAS residue (i.e., ground GAS shell and meat residue) to the effects of adding lime upon soil properties and microbes in a greenhouse pot experiment. Each pot was incubated for 120 days, and soil pH, nutrients, microbial species, and enzyme activity were assessed. Results showed that addition of GAS residue significantly improved soil pH, contents of total organic carbon (TOC), total nitrogen (TN), total phosphorus (TP), and available nitrogen but decreased soil available phosphorus (AP) content due to phosphorus sorption induced by soil organic matter (OM) and high pH. The GAS residue added to soil released nutrients and alleviated soil acidity, as well as provided more resources to soil microbes to increase their bioactivity, although lime addition was better at mitigating soil acidity. We found that with added GAS residue of 25 g kg−1, the soil nitrate nitrogen (NO3-N) content increased by 10 times; microbial biomass increased by 43%; and enzyme activity of β-1,4-glucosidase, β-1,4-N-acetylglucosaminidase, and β-d-cellobiosidase also were enhanced, compared to the control. Our findings suggest that GAS residue functions well as a fertilizer and soil amendment to aid the remediation of barren and acidic soils, making it a valuable and useful option in the control of the invasive GAS.

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Abbreviations

NH4-N:

Ammonium nitrogen

NO3-N:

Nitrate nitrogen

TP:

Total phosphorus

TOC:

Total organic carbon

TN:

Total nitrogen

AP:

Available phosphorus

G+:

Gram-positive bacteria

G−:

Gram-negative bacteria

A:

Actinomycetes

B:

Bacteria (the sum of G+ and G−)

F:

Fungi

BG:

β-1,4-Glucosidase

CB:

β-d-Cellobiosidase

NAG:

β-1,4-N-acetylglucosaminidase

ACP:

Acid phosphatase

References

  1. Acosta-Martinez V, Tabatabai M (2000) Enzyme activities in a limed agricultural soil. Biol Fertil Soils 31:85–91

  2. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944

  3. Andersen J (1976) An ignition method for determination of total phosphorus in lake sediments. Water Res 10:329–331

  4. Attademo AM, Lajmanovich RC, Peltzer PM, Junges CM (2016) Acute toxicity of metaldehyde in the invasive rice snail Pomacea canaliculata and sublethal effects on tadpoles of a non-target species (Rhinella arenarum). Water Air Soil Pollut 227:400

  5. Bååth E, Anderson T-H (2003) Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA-based techniques. Soil Biol Biochem 35:955–963

  6. Bell CW, Fricks BE, Rocca JD, Steinweg JM, McMahon SK, Wallenstein MD (2013) High-throughput fluorometric measurement of potential soil extracellular enzyme activities. J Vis Exp 81:1–16

  7. Bombeo-Tuburan I, Fukumoto S, Rodriguez E (1995) Use of the golden apple snail, cassava, and maize as feeds for the tiger shrimp, Penaeus monodon, in ponds. Aquaculture 131:91–100

  8. Boot CM, Hall EK, Denef K, Baron JS (2016) Long-term reactive nitrogen loading alters soil carbon and microbial community properties in a subalpine forest ecosystem. Soil Biol Biochem 92:211–220

  9. Bossio DA, Scow K (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278

  10. Bowles TM, Acosta-Martínez V, Calderón F, Jackson LE (2014) Soil enzyme activities, microbial communities, and carbon and nitrogen availability in organic agroecosystems across an intensively-managed agricultural landscape. Soil Biol Biochem 68:252–262

  11. Bray RH, Kurtz L (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46

  12. Calumpang S, Medina M, Tejada A, Medina J (1995) Environmental impact of two molluscicides: niclosamide and metaldehyde in a rice paddy ecosystem. Bull Environ Contam Toxicol 55:494–501

  13. Carlsson NO, Brönmark C, Hansson L-A (2004) Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands. Ecology 85:1575–1580

  14. Castle GD, Mills GA, Gravell A, Jones L, Townsend I, Cameron DG, Fones GR (2017) Review of the molluscicide metaldehyde in the environment. Environ Sci Water Res Technol 3:415–428

  15. Cayuela M, Sinicco T, Mondini C (2009) Mineralization dynamics and biochemical properties during initial decomposition of plant and animal residues in soil. Appl Soil Ecol 41:118–127

  16. Chapin CT, Bridgham SD, Pastor J, Updegraff K (2003) Nitrogen, phosphorus, and carbon mineralization in response to nutrient and lime additions in peatlands. Soil Sci 168:409–420

  17. Chiu Y-W, Wu J-P, Hsieh T-C, Liang S-H, Chen C-M, Huang D-J (2014) Alterations of biochemical indicators in hepatopancreas of the golden apple snail, Pomacea canaliculata, from paddy fields in Taiwan. J Environ Biol 35:667–673

  18. Dancer W, Peterson L, Chesters G (1973) Ammonification and nitrification of N as influenced by soil pH and previous N treatments 1. Soil Sci Soc Am J 37:67–69

  19. Debicka M, Kocowicz A, Weber J, Jamroz E (2016) Organic matter effects on phosphorus sorption in sandy soils. Arch Agron Soil Sci 62:840–855

  20. Dong L, Lin L, Li Q, Huang Z, Tang X, Wu M, Li C, Cao X, Scholz M (2018) Enhanced nitrate-nitrogen removal by modified attapulgite-supported nanoscale zero-valent iron treating simulated groundwater. J Environ Manag 213:151–158

  21. Erisman JW, Bleeker A, Hensen A, Vermeulen A (2008) Agricultural air quality in Europe and the future perspectives. Atmos Environ 42:3209–3217

  22. Geisseler D, Horwath WR (2009) Relationship between carbon and nitrogen availability and extracellular enzyme activities in soil. Pedobiologia 53:87–98

  23. Gérard F (2016) Clay minerals, iron/aluminum oxides, and their contribution to phosphate sorption in soils—a myth revisited. Geoderma 262:213–226

  24. Gooding EL, Fowler AE, Knott D, Dillon RT, Brown T, Kendrick MR, Kingsley-Smith PR (2018) Life history and phenological characteristics of the invasive Island apple snail Pomacea maculata (Perry, 1810) in stormwater retention ponds in coastal South Carolina, USA. J Shellfish Res 37:229–239

  25. Goulding, K., Annis, B., 1998. Lime, liming and the management of soil acidity. Proceedings-Fertiliser Society (United Kingdom) 410, 1-36

  26. Guo JH, Liu XJ, Zhang Y, Shen J, Han W, Zhang W, Christie P, Goulding K, Vitousek P, Zhang F (2010) Significant acidification in major Chinese croplands. Science 327:1008–1010

  27. Hale BK, Herms DA, Hansen RC, Clausen TP, Arnold D (2005) Effects of drought stress and nutrient availability on dry matter allocation, phenolic glycosides, and rapid induced resistance of poplar to two lymantriid defoliators. J Chem Ecol 31:2601–2620

  28. Hallett KC, Atfield A, Comber S, Hutchinson TH (2016) Developmental toxicity of metaldehyde in the embryos of Lymnaea stagnalis (Gastropoda: Pulmonata) co-exposed to the synergist piperonyl butoxide. Sci Total Environ 543:37–43

  29. Halwart M (1994) The golden apple snail Pomacea canaliculata in Asian rice farming systems: present impact and future threat. Int J Pest Manag 40:199–206

  30. Haynes RJ, Zhou Y-F (2018) Effect of pH and added slag on the extractability of Si in two Si-deficient sugarcane soils. Chemosphere 193:431–437

  31. Hu Y, Schmidhalter U (2005) Drought and salinity: a comparison of their effects on mineral nutrition of plants. J Plant Nutr Soil Sci 168:541–549

  32. Huang H-C, Liao S-C, Chang F-R, Kuo Y-H, Wu Y-C (2003) Molluscicidal Saponins from Sapindus mukorossi, inhibitory agents of Golden apple snails, Pomacea canaliculata. J Agric Food Chem 51:4916–4919

  33. Ibrahim R, Haiyee Z, Latip S (2017) The antifeedant activity of essential oil from Cymbopogon citratus and Piper bitle for controlling golden apple snail, Pomacea canaliculata. J Fundamental Appl Sci 9:39–49

  34. Joshi RC, San Martín R, Saez-Navarrete C, Alarcon J, Sainz J, Antolin MM, Martin AR, Sebastian LS (2008) Efficacy of quinoa (Chenopodium quinoa) saponins against golden apple snail (Pomacea canaliculata) in the Philippines under laboratory conditions. Crop Prot 27:553–557

  35. Keenan SW, Schaeffer SM, Jin VL, DeBruyn JM (2018) Mortality hotspots: nitrogen cycling in forest soils during vertebrate decomposition. Soil Biol Biochem 121:165–176

  36. Kumar A, Walia BS, Bajaj A (2007) Influence of fly ash, lime, and polyester fibers on compaction and strength properties of expansive soil. J Mater Civ Eng 19:242–248

  37. Lee CH, Lee DK, Ali MA, Kim PJ (2008) Effects of oyster shell on soil chemical and biological properties and cabbage productivity as a liming materials. Waste Manag 28:2702–2708

  38. Leff JW, Jones SE, Prober SM, Barberán A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JM (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci 112:10967–10972

  39. Litsinger J, Estano DB (1993) Management of the golden apple snail Pomacea canaliculata (Lamarck) in rice. Crop Prot 12:363–370

  40. Mahimairaja S, Bolan N, Hedley M, Macgregor A (1994) Losses and transformation of nitrogen during composting of poultry manure with different amendments: an incubation experiment. Bioresour Technol 47:265–273

  41. Mariani L, Chang SX, Kabzems R (2006) Effects of tree harvesting, forest floor removal, and compaction on soil microbial biomass, microbial respiration, and N availability in a boreal aspen forest in British Columbia. Soil Biol Biochem 38:1734–1744

  42. Marsyha, D., Wijayanti, H., Anjani, G., 2018. Contribution of golden apple snail flour to enhance omega-3 and omega-6 fatty acids contents in weaning food. IOP Conference Series: Earth and Environmental Science. IOP Publishing, p. 012075

  43. Miransari M, Bahrami H, Rejali F, Malakouti M (2009) Effects of arbuscular mycorrhiza, soil sterilization, and soil compaction on wheat (Triticum aestivum L.) nutrients uptake. Soil Tillage Res 104:48–55

  44. Mochida O (1991) Spread of freshwater Pomacea snails (Pilidae, Mollusca) from Argentina to Asia. Micronesica 3:51–62

  45. Olivier HM, Jenkins JA, Berhow M, Carter J (2016) A pilot study testing a natural and a synthetic molluscicide for controlling invasive apple snails (Pomacea maculata). Bull Environ Contam Toxicol 96:289–294

  46. Ostrowska A, Porębska G (2012) Assessment of TOC-SOM and SOM-TOC conversion in forest soil. Pol J Environ Stud 21:1767–1775

  47. Pal SK (2011) Phosphorus sorption-desorption characteristics of soils under different land use patterns of eastern India. Arch Agron Soil Sci 57:365–376

  48. Palis F, Macatula R, Browning L (1997) Bayluscide 250 EC (Niclosamide), an effective molluscicide for the golden apple snail (Pomacea canaliculata Lamarck) control in the Philippine rice production system. Philipp J Crop Sci 22:41–52

  49. Pan B, Lam SK, Mosier A, Luo Y, Chen D (2016) Ammonia volatilization from synthetic fertilizers and its mitigation strategies: a global synthesis. Agric Ecosyst Environ 232:283–289

  50. Pietri JA, Brookes P (2008) Relationships between soil pH and microbial properties in a UK arable soil. Soil Biol Biochem 40:1856–1861

  51. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

  52. Ramdwar M, Stoute V, Potts J (2018) The influence of commercial food grade essences on the efficacy of metaldehyde for the control of Achatina (Lissachatina) fulica (Bowdich). Cogent Food Agric 4:1–17

  53. Ren L, Cai C, Zhang J, Yang Y, Wu G, Luo L, Huang H, Zhou Y, Qin P, Yu M (2018) Key environmental factors to variation of ammonia-oxidizing archaea community and potential ammonia oxidation rate during agricultural waste composting. Bioresour Technol 270:278–285

  54. Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340

  55. San Martín R, Ndjoko K, Hostettmann K (2008) Novel molluscicide against Pomacea canaliculata based on quinoa (Chenopodium quinoa) saponins. Crop Prot 27:310–319

  56. Schipanski ME, Drinkwater LE (2012) Nitrogen fixation in annual and perennial legume-grass mixtures across a fertility gradient. Plant Soil 357:147–159

  57. Schlich K, Hund-Rinke K (2015) Influence of soil properties on the effect of silver nanomaterials on microbial activity in five soils. Environ Pollut 196:321–330

  58. Smith JL, Halvorson JJ, Bolton H Jr (2002) Soil properties and microbial activity across a 500 m elevation gradient in a semi-arid environment. Soil Biol Biochem 34:1749–1757

  59. Smith P, House JI, Bustamante M, Sobocká J, Harper R, Pan G, West PC, Clark JM, Adhya T, Rumpel C (2016) Global change pressures on soils from land use and management. Glob Chang Biol 22:1008–1028

  60. Sumner ME, Noble AD (2003) Soil acidification: the world story. In: Handbook of soil acidity. Marcel Dekker, New York, pp 1–28

  61. Takougang I, Meli J, Wabo Poné J, Angwafo F (2007) Community acceptability of the use of low-dose niclosamide (Bayluscide®), as a molluscicide in the control of human schistosomiasis in Sahelian Cameroon. Ann Trop Med Parasitol 101:479–486

  62. Tasoff J, Mee MT, Wang HH (2015) An economic framework of microbial trade. PLoS One 10

  63. Van Breemen N, Burrough P, Velthorst Ev, Van Dobben H, de Wit T, Ridder Td, Reijnders H (1982) Soil acidification from atmospheric ammonium sulphate in forest canopy throughfall. Nature 299:548–550

  64. Wei H, Chen X, He J, Zhang J, Shen W (2017) Exogenous nitrogen addition reduced the temperature sensitivity of microbial respiration without altering the microbial community composition. Front Microbiol:8

  65. White D, Davis W, Nickels J, King J, Bobbie R (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40:51–62

  66. Woodley A, Drury C, Yang X, Reynolds W, Calder W, Oloya T (2018) Streaming urea ammonium nitrate with or without enhanced efficiency products impacted corn yields, ammonia, and nitrous oxide emissions. Agron J 110:444–454

  67. Xing J, Wang H, Brookes PC, Salles JF, Xu J (2019) Soil pH and microbial diversity constrain the survival of E. coli in soil. Soil Biol Biochem 128:139–149

  68. Yan X, Wang D, Zhang H, Zhang G, Wei Z (2013) Organic amendments affect phosphorus sorption characteristics in a paddy soil. Agric Ecosyst Environ 175:47–53

  69. Zhalnina K, Dias R, de Quadros PD, Davis-Richardson A, Camargo FA, Clark IM, McGrath SP, Hirsch PR, Triplett EW (2015) Soil pH determines microbial diversity and composition in the park grass experiment. Microb Ecol 69:395–406

  70. Zhou J, Jiang X, Zhou B, Zhao B, Ma M, Guan D, Li J, Chen S, Cao F, Shen D (2016) Thirty four years of nitrogen fertilization decreases fungal diversity and alters fungal community composition in black soil in northeast China. Soil Biol Biochem 95:135–143

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Acknowledgments

We are thankful for anonymous reviewers’ constructive comments and kind help for the improvement of the manuscript.

Funding

We received financial support from the National Natural Science Foundation of China (No. 31870525, No. U1701236, No. 41871034), Guangdong Provincial Key Laboratory of Eco-Circular Agriculture (No. 2019B030301007), and Guangdong Modern Agricultural Technology Innovation Team Construction Project (No. 2018LM1100, 2019KJ105).

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Correspondence to Jiaen Zhang.

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Jiaxin Wang and Xuening Lu are equally contributing authors.

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Wang, J., Lu, X., Zhang, J. et al. Using golden apple snail to mitigate its invasion and improve soil quality: a biocontrol approach. Environ Sci Pollut Res (2020). https://doi.org/10.1007/s11356-020-07998-9

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Keywords

  • Biocontrol
  • Golden apple snail
  • Microbial community
  • Soil nutrients
  • Soil pH
  • Waste management