Abstract
Purpose
The vertical distribution of phosphorus (P) can vary depending on specific environmental factors like type of water body, soil type, land management and bioturbating macrofauna. To investigate how the benthic macrofauna affects vertical P distribution in aquatic sediment, a mesocosm laboratory experiment was conducted by using two muluscans: Bellamya aeruginosa and Corbicula fluminea.
Materials and method
A 21-day mesocosm experiment was conducted with natural assemblages of two benthic macroinvertebrates (B. aeruginosa and C. fluminea). The Standard Measurements and Testing (SMT) method was used to acquire the migration, distribution, and transformation of P forms in benthic sediment bioturbation.
Results and discussion
Results showed that the bioturbation of the benthic animals affected the decomposition and transformation of organic P (OP) in the sediment. The OP content in the sediment treated with benthic animal groups decreased dramatically during the experiment (p < 0.05). The non-apatite-inorganic-P (NAIP), inorganic-P (IP), and total-P (TP) of all treatment groups in the sediment layers increased over the experimental period. Comparing the two forms of bioturbation exerted, that of C. fluminea was significantly stronger compared to B. aeruginosa and the control groups. The apatite P content increased significantly in the 0–1-cm layer, and a significant decrease was observed in the 1–2-cm layer of the sediment (p < 0.05).
Conclusion
This study shows that the bioturbation forces created by benthic macroinvertebrates B. aeruginosa and C. fluminea have significant impacts on the vertical distribution and transformation of sediment P forms and that the bioturbation effects of the C. fluminea on migration/transformation of P forms was stronger compared to B. aeruginosa.
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Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Ahlgren J, Reitzel K, De Brabandere H, Gogoll A, Rydin E (2011) Release of organic P forms from lake sediments. Water Res 45(2):565–572. https://doi.org/10.1016/j.watres.2010.09.020
Auld JR, Jarne P (2016) Encyclopedia of Evolutionary Biology
Baldwin SD (2013) Organic phosphorus in the aquatic environment. Environ Chem 10:439–454. https://doi.org/10.1071/EN13151
Bartoli M, Benelli S, Magri M et al (2020) Contrasting effects of bioturbation studied in intact and reconstructed estuarine sediments. Water 12(11):3125. https://doi.org/10.3390/w12113125
Bellier N, Chazarenc F, Comeau Y (2006) Phosphorus removal from wastewater by mineral apatite. Water Res 40(15):2965–2971. https://doi.org/10.1016/j.watres.2006.05.016
Berezina NA, Maximov AA, Vladimirova OM (2019) Influence of benthic invertebrates on phosphorus flux at the sediment-water interface in the easternmost Baltic Sea. Mar Ecol Prog Ser 608:33–43. https://doi.org/10.3354/meps12824
Boyd CE (2015) Phosphorus. In: Water quality. Springer, Cham. https://doi.org/10.1007/978-3-319-17446-4_12
Chislock MF, Doster E, Zitomer RA, Wilson AE (2013) Eutrophication: causes, consequences, and controls in aquatic ecosystems. Nat Sci Educ 4(4):10
Chon K, KyongShon H, Cho J (2012) Membrane bioreactor and nanofiltration hybrid system for reclamation of municipal wastewater: Removal of nutrients, organic matter and micropollutants. Bioresour Technol 122:181–188. https://doi.org/10.1016/j.biortech.2012.04.048
Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323:1014–1015
Diaz OA, Reddy KR, Moore PA Jr (1994) Solubility of inorganic phosphorus in stream water as influenced by pH and calcium concentration. Water Res 28(8):1755–1763. https://doi.org/10.1016/0043-1354(94)90248-8
Edlund G, Carman R (2001) Distribution and diagenesis of organic and inorganic phosphorus in sediments of the Baltic proper. Chemosphere 45(6–7):1053–1061
Heilskov AC (2001) Effects of benthic fauna on organic matter mineralization in fish-farm sediments: importance of size and abundance. J Marine Sci 58(2):427–434. https://doi.org/10.1006/jmsc.2000.1026
Heiri O, Lotter AF, Lemcke G (2001) Loss on ignition as a method for estimating organic and carbonate content in sediments: reproducibility and comparability of results. J Paleolimnol 25:101–110
Huang QH, Wang ZJ, Wang DH, Wang C, Ma M, Jin XC (2005) Origins and mobility of phosphorus forms in the sediments of Lakes Taihu and Chaohu. China J Environ Sci Heal A 40(1):91–102. https://doi.org/10.1081/ese-200033593
Jin X, Jiang X, Yao Y, Li L, Fengchang W (2006) Effects of organisms on the release of phosphorus at the interface between sediment and water. Water Environ Res 78(12):2405–2259. https://doi.org/10.2307/25053647
Kapiti D, Bekteshi A (2014) Phosphorus bioavailability in sediments of a sludge-disposal Shkodra Lake. J Environ Prot Ecol 15(1):48–52
Kozyrev R, Umezawa Y, Yoh M (2023) Total phosphorus and phosphorus forms change in sediments along the Tone River. Front Earth Sci 11:1060312. https://doi.org/10.3389/feart.2023.1060312
Kristensen E, Neto JM, Lundkvist M, Frederiksen L, Pardal MÂ, Valdemarsen T, Rene Flindt M (2013) Influence of benthic macroinvertebrates on the erodibility of estuarine cohesive sediments: density- and biomass-specific responses. Estuar Coast Shelf Sci 134:80–87. https://doi.org/10.1016/j.ecss.2013.09.020
Lepori F, Capelli C (2021) Effects of phosphorus control on primary productivity and deep-water oxygenation: insights from Lake Lugano (Switzerland and Italy). Hydrobiologia 848:613–629. https://doi.org/10.1007/s10750-020-04467-9
Lewandowski J, Hupfer M (2005) Effect of macrozoobenthos on two-dimensional small-scale heterogeneity of pore water phosphorus concentrations in lake sediments: a laboratory study. Limnol Oceanogr 50(4):1106–1118
Li DP, Huang Y (2010) Sedimentary phosphorus fractions and bioavailability as influenced by repeated sediment resuspension. Ecol Eng 36:958–962. https://doi.org/10.1016/j.ecoleng.2010.04.014
Li RF, Tan WB, Gao RT, Huang CH, Zhang H, Li D (2018) Distribution characteristics of organic matter, nitrogen and phosphorus in Sediments of Xiao River. J Environ Eng Techn 8:241–247
Liu C, Hu N, Song W, Chen Q, Zhu L (2019) Aquaculture feeds can be outlaws for eutrophication when hidden in rice fields? A case study in Qianjiang, China. Int J Environ Res Public Health 16(22):4471. PMCID: PMC6887982, PMID: 31766308; 2019. https://doi.org/10.3390/ijerph16224471
Liu XS, Zhang KX, Lv J et al (2010) The effect of Bellamya aeruginosa on physical and chemical properties of the algal blooms water. Ecol Sci 29(5):438–443
Long Z, Ji Z, Pei Y (2023) Characteristics and distribution of phosphorus in surface sediments of a shallow lake Author links open overlay panel J Environ Sci 124:50–60. https://doi.org/10.1016/j.jes.2021.10.012
López-Alonso R, Sánchez O, Fernández-Rodríguez I, Arias A (2022) Diversity and distribution of bivalve molluscs in the Central Cantabrian Sea and the Avilés Canyons System (Bay of Biscay). Estuar Coast Shelf Sc 273(31):107907. https://doi.org/10.1016/j.ecss.2022.107907
Lukwambe B, Yang W, Zheng Y, Nicholaus R, Zhu J, Zheng Z (2018) Bioturbation by the razor clam (Sinonovacula constricta) on the microbial community and enzymatic activities in the sediment of an ecological aquaculture wastewater treatment system. Sci Total Environ 643:1098–1107. https://doi.org/10.1016/j.scitotenv.2018.06.251
Mainstone C, Parr W (2002) Phosphorus in rivers — ecology and management. Sci Total Environ 282:25–47. https://doi.org/10.1016/S0048-9697(01)00937-8
McKindsey CW, Archambault P, Callier MD, Olivier F (2011) Influence of suspended and off-bottom mussel culture on the sea bottom and benthic habitats: a review. Can J Zool 89:622–646
Meysman FJ, Middelburg JJ, Heip CH (2006) Bioturbation: a fresh look at Darwin’s last idea. Trends Ecol Evol 21(12):688–695
Michaud E, Desrosiers G, Mermillod-Bondin F, Sundby B, Stora G (2006) The functional group approach to bioturbation: II, the Effects of the Macoma balthica community on fluxes of nutrients and dissolved organic carbon across the sediment-water interface. J Exp Mar Biol Ecol 337:178–189. https://doi.org/10.1016/j.jembe.2006.06.025
Mo S, Zhang X, Tang Y et al (2017) Effects of snails, submerged plants and their coexistence on eutrophication in aquatic ecosystems. Knowl Manag Aquat Ecosyst 418:44
Molle P, Liénard A, Grasmick A, Iwema A, Kabbabi A (2005) Apatite as an interesting seed to remove phosphorus from wastewater in constructed wetlands. Water Sci Technol 51(9):193–203. https://doi.org/10.2166/wst.2005.0318
Ngatia L, Taylor R (2019) Phosphorus eutrophication and mitigation strategies. Phosphorus — recovery and recycling. https://doi.org/10.5772/intechopen.79173
Nicholaus R, Lukwambe B, Mwakalapa EB, Yang W, Zhu J, Zheng Z (2020a) Impacts of bioturbation by Venus clam Cyclina sinensis (Gmelin, 1791) on benthic metabolism and sediment nutrient dynamics in a shrimp-clam polyculture pond. Indian J Fish 67(3). https://doi.org/10.21077/ijf.2020.67.3.79036-04
Nicholaus R, Lukwambe B, Yang W, Zhu J, Zheng Z (2020b) In situ assemblies of bacteria and nutrient dynamics in response to an ecosystem engineer, marine clam Scapharca subcrenata, in the sediment of an aquaculture bioremediation system. J Ocean Univ China 19:1447–1460. https://doi.org/10.1007/s11802-020-4464-7
Nicholaus R, Lukwambe B, Zhao L, Yang W, Zhu J, Zheng Z (2019) Bioturbation of blood clam Tegillarca granosa on benthic nutrient fluxes and microbial community in an aquaculture wastewater treatment system. Int Biodeterior Biodegrad 142:73–82. https://doi.org/10.1016/j.ibiod.2019.05.004
Nicholaus R, Zheng Z (2014) The effects of bioturbation by the Venus clam Cyclina sinensis on the fluxes of nutrients across the sediment–water interface in aquaculture ponds. Aquac Inter 22(2):913–924. https://doi.org/10.1007/s10499-013-9716-8
Niu J, Zhang T, Wen G, Zheng Z, Jia Y, Tan CS, Welackey T (2023) Agronomic approach to evaluate the nitrogen use efficiency of liquid, solid, and composted swine manures in corn–soybean rotation. Front Environ Sci 11:1–11. https://doi.org/10.3389/fenvs.2023.1021890
Peng H, Jiang A, Wang H (2021) Adsorption and desorption characteristics of phosphorus on sediments in Panzhihua section of Jinsha River, China. IOP Conf Ser Earth Environ Sci 651:042059. https://doi.org/10.1088/1755-1315/651/4/042059
Qian Y, Liang X, Chen Y, Lou L, Cui X, Tang J, Li P, Cao R (2011) Significance of biological effects on phosphorus transformation processes at the water–sediment interface under different environmental conditions. Ecol Eng 37(6):816–825. https://doi.org/10.1016/j.ecoleng.2010.12.005
Ruban V, López-Sánchez JF, Pardo P et al (2001) Harmonized protocol and certified reference material for the determination of extractable contents of phosphorus in freshwater sediments — a synthesis of recent works. Fresenius J Anal Chem 370(2–3):224–228. https://doi.org/10.1007/s002160100753
Ruban V, López-Sánchez JF, Pardo P, Rauret G, Muntau H, Quevauviller P (1999) Selection and evaluation of sequential extraction procedures for the determination of phosphorus forms in lake sediment. J Environ Monitor 1(1):51–56. https://doi.org/10.1039/a807778i
Rydin E (2000) Potentially mobile phosphorus in Lake Erken sediment. Water Res 34:2037–2042. https://doi.org/10.1016/S0043-1354(99)00375-9
Sanz-Lázaro C, Belando MB, Marín-Guirao L, Navarrete-Mier F; Marín A (2011) Relationship between sedimentation rates and benthic impact on Maërl beds derived from fish farming in the Mediterranean. Mar Environ Res 71(1):22–30. https://doi.org/10.1016/j.marenvres.2010.09.005
Sardans J, Janssens IA, Ciais P, Obersteiner M, Peñuelas J (2021) Recent advances and future research in ecological stoichiometry. Perspect. Plant Ecol Evol Syst 50:125611. https://doi.org/10.1016/j.ppees.2021.125611
Schindler DW (2006) Recent advances in the understanding and management of eutrophication. Limnol Oceanogr 51:356–363. https://doi.org/10.4319/lo.2006.51.1_part_2.0356
Selig U (2003) Particle size-related phosphate binding and P-release at the sediment–water interface in a shallow German lake. Hydrobiologia 492:107–118. https://doi.org/10.1023/A:1024865828601
Shen RJ, Gu XH, Chen HH, Mao ZG, Zeng QF, Jeppesen E (2020a) Combining bivalve (Corbicula fluminea) and filter-feeding fish (Aristichthys nobilis) enhances the bioremediation effect of algae: an outdoor mesocosm study. Sci Total Environ 727:138692
Shen X, Yuan N, Wang C (2020b) The bioturbation effect of the snail Bellamya aeruginosa on phosphorus immobilisation by drinking water treatment residue in sediment. A long-term continuous flow test. J Environ Manage 266:110579. https://doi.org/10.1016/j.jenvman.2020.110579
Shi L, Wang D, Qian L, Hellio C, Fauchon M, Trepos R et al (2020) Reduction of potential ennoblement of stainless steel in natural seawater by an ecofriendly biopolymer. J Environ Chem Eng 8(1):103609. https://doi.org/10.1016/j.jece.2019.103609
Sousa R, Antunes C, Guilhermino L (2008) Ecology of the invasive Asian clam Corbicula fluminea (Müller, 1774) in aquatic ecosystems: an overview. Ann Limnol Int J Lim 44:85–94
Sousa R, Gutiérrez JL, Aldridge DC (2009) Non-indigenous invasive bivalves as ecosystem engineers. Biol Invasions 11:2367–2385. https://doi.org/10.1007/s10530-009-9422
Strong EE, Gargominy O, Ponder WF, Bouchet P (2007) Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. In: Balian EV, Lévêque C, Segers H, Martens K (eds) Freshwater animal diversity assessment. Developments in hydrobiology, vol 198. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8259-7_17
Su J, van Bochove E, Auclair JC, Thériault G, Hu C, Li X (2014) Phosphorus fluxes at the sediment-water interface in a temperate region agricultural catchment. Water Air Soil Poll 225(1):1–11
Suratissa DM, Rathnayake U (2017) Effect of pollution on diversity of marine gastropods and its role in trophic structure at Nasese shore, Suva, Fiji Islands. J Asia Pac Biodivers. https://doi.org/10.1016/j.japb.2017.02.001
Tang BJ, Chen L, Jiang X et al (2009) Phosphorus speciation in sediment and their relationship with soluble phosphorus concentrations in porewater in Lake Chaohu. J Agro-Environ Sci 28(9):1867–1873
Tufekci V, Balkis N, Beken CP, Ediger D, Mantikci M (2010) Phytoplankton composition and environmental conditions of a mucilage event in the Sea of Marmara. Turk J Biol 32:199–210. https://doi.org/10.3906/biy-0812-1
Uusitalo R, Yli-Halla M, Turtola E (2000) Suspended soil as a source of potentially bioavailable phosphorus in surface runoff waters from clay soils. Water Res 34(2000):2477–2482. https://doi.org/10.1016/S0043-1354(99)00419-4
van de Velde Rebecca SJ, James K, Callebaut I, Hidalgo-Martinez S, Meysman FJR (2021) Bioturbation has a limited effect on phosphorus burial in salt marsh sediments. Biogeosciences 18:1451–1461. https://doi.org/10.5194/bg-18-1451-2021
Weigelhofer G, Hein T, Bondar-Kunze E (2018) Phosphorus and nitrogen dynamics in riverine systems: human impacts and management options. Riverine ecosystem management. Aquat Ecol Ser 8:187–202. https://doi.org/10.1007/978-3-319-73250-3_10
Yang Y, Zhang J, Liu L, Wang G, Chen M, Zhang Y, Tang X (2020) Experimental study on phosphorus release from sediment with fresh-water snail (Bellamya aeruginosa) bioturbation in eutrophic lakes. J Soils Sediments 20(5):2526–2536. https://doi.org/10.1007/s11368-020-02614-2
Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Penuelas J, Richter A, Sardans J, et al. (2015) The application of ecological stoichiometry to plant-microbial-soil organic matter transformations. Ecol Monogr 85:133–155
Zhan ZL, Yang Y, Song W et al (2007) The influence of microorganisms on total phosphorus of sediments from Lake Taihu. Henan Sci 25(5):839–841
Zhang L, Liao Q, He W et al (2013) The effects of temperature on oxygen uptake and nutrient flux in sediment inhabited by molluscs. J Limnol 72(1):13–20
Zhao L, Zheng Y, Nicholaus R et al (2019) Bioturbation by the razor clam Sinonovacula constricta affects benthic nutrient fluxes in aquaculture wastewater treatment ecosystems. Aquacult Environ 11:87–96. https://doi.org/10.3354/aei00298
Zheng Z, Lv J, Lu K, Jin C, Zhu J, Liu X (2011) The impact of snail (Bellamya aeruginosa) bioturbation on sediment characteristics and organic carbon fluxes in an eutrophic pond. Clean-Soil Air Water 39:566–571. https://doi.org/10.1002/clen.201000212
Zhou QX, Gibson CE, Zhu YM (2001) Evaluation of phosphorus bioavailability in sediments of three contrasting lakes in China and the UK. Chemosphere 42:221–225. https://doi.org/10.1016/s0045-6535(00)00129-6
Zhou Y, Song C, Cao X, Li J, Chen G, Xia Z, Jiang P (2008) Phosphorus fractions and alkaline phosphatase activity in sediments of a large eutrophic Chinese lake (Lake Taihu). Hydrobiologia 599:119–125. https://doi.org/10.1007/s10750-007-9185-z
Zhu J, Lu K, Liu X (2013) Can the freshwater snail Bellamya aeruginosa (Mollusca) affect phytoplankton community and water quality. Hydrobiologia 707(1):147–157. https://doi.org/10.1007/s10750-012-1417-1
Zhu XL, Gu J, Jin H et al (2015) Effects of Corbicula fluminea in Lake Taihu on the improvement of eutrophic water quality. J Lake Sci 27(3):486–492. https://doi.org/10.18307/2015.0316
Funding
This study was supported by the National Key R & D Program of China (2020YFD0900201), the Zhejiang Public Welfare Technology Research Program of China (ZPWTP) (LGN18C190008), and the K.C. Wong Magna Fund in Ningbo University.
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Nicholaus, R., Lukwambe, B. & Zheng, Z. Effects of Bellamya aeruginosa and Corbicula fluminea bioturbation on the vertical distribution of phosphorus forms in aquatic sediments: a laboratory study. J Soils Sediments 24, 1019–1029 (2024). https://doi.org/10.1007/s11368-023-03686-6
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DOI: https://doi.org/10.1007/s11368-023-03686-6