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Abstract As an important factor influencing the physical， chemical and biological processes of sediments， the bioturbation of macrobenthos has received extensive attention in the study of the biogeochemical processes of sediments. However， previous studies provided limited scope for the effects of the bioturbation on the biogeochemical processes of sediments. Based on the analysis of recently published data， this paper presented an integrated overview to summarize the forms of bioturbation （rework， bioirrigation， biodeposition， bioresuspension， biodiffusion）， and the effects of bioturbation on the organic matter decomposition， microorganisms， and nutrient flux at the sediment-water interface. To better understand the impacts of bioturbation on biogeochemical processes of sediments， the research should be strengthened in the following aspects in the future： the combination of field experiment and lab simulation test should be strengthened as for the research method; much more attention should be paid to the other sea areas besides hot sea areas and different ecosystems regarding the research area; and the biogenic elements except nitrogen and phosphorus， microorganisms， and heavy metals should be deepened regarding the research content.
Key words Organic matter decomposition; Microorganism; Sediment-water interface; Bioturbation
Bioturbation is one of the key ecological processes in estuaries， near shore and shallow waters. Bioturbation refers to the change of solute exchange and particle migration in sediments and sediment-water interface of macrobenthos during their life activities （such as feeding， excretion， burrowing and movement）[1]. The importance of bioturbation was first proposed by Darwin in 1891. A series of subsequent studies confirmed Darwins view and further revealed the important role and significance of bioturbation in benthic ecosystem and geological evolution[2]. However， the bioturbation of macrobenthos and their effects on biogeochemical processes in sediments have not been systematically organized. Thus， the forms of bioturbation and the effects of bioturbation on biogeochemical cycling process in sediments were summarized in order to improve the knowledge system of bioturbation.
Forms of Bioturbation
Rework
Bioturbation fundamentally change the physical and chemical characteristics of sediment， accelerating the material exchange between pore water and overlying water. Thereby， this process affects the stability and erosion rate of sediment， changing the pore rate and surface composition of sediment. Macrobenthos （especially crustaceans） have a strong ability to transform the sediment environment and are called ecosystem engineer. Although these species may not be dominant in number in the community， their strong activity ability， burrowing life habit， and great alteration of sediments can eventually cause fundamental changes in the process of biogeochemistry in sediments. Rhoads[3] observed that a sediment-feeding mollusk （Yoldia Limatula） was able to modify the sediment structure at a rate of up to 50 L/（m2·yr）. Bioirrigation
As a result of respiration or other activities， burrowing macrobenthos can produce rapid water flow in the cave， so that the material diffusion between the overlying water， the deep sediment and pore water can be completed through the cave. This process of material exchange between the overlying water and deep sediment is called bioirrigation. Bioirrigation can transfer dissolved oxygen to deep sediments， thus accelerating the degradation of organic matter. In addition， this process affects the sediment-water interface material exchange.
Biodeposition
Filter-feeding macrobenthos feed on plankton and organic debris in the water layer. In the process of filter feeding， a large number of particles in the water layer are filtered and trapped， and then new sediment is formed in the form of large particles such as feces or pseudofeces. This process is called biological deposition because it speeds up the deposition process of particulate matter in the water layer. Haven and Morales-Alamo[4] calculated that 0.4 hm2 oyster farm in the York estuary could produced 981 kg of feces or pseudofeces per week. In the Queule estuary in Chile， the biodeposition rate of shellfish to organic matter in the water reached 49 g·DW/（m2·d）[5].
Bioresuspension
Macrobenthos produce water flow during burrowing， feeding and excretion， and the process of returning sedimentary particles to the water layer in suspension is called bioresuspension. Zaiko and Olenin[6] verified the possibility of biological resuspension in the laboratory. Bioresuspension is related to the water flow rate at the sediment-water interface. Due to the limitation of research methods， experimental data on bioresuspension are still lacking.
Biodiffusion
Macrobenthos can cause small range of diffusion of sediment and pore water in the process of biological activities， which is called biodiffusion. Experiments have confirmed that the biological activities of different macrobenthos cloud accelerated the diffusion process of sediment particles and pore water. Compared with bioirrigation， however， biodiffusion only involves the short distance migration of materials.
Effects of Bioturbation on the Biogeochemical Cycle in Sediments
Effects on organic matter decomposition
It has been demonstrated that bioturbation promoted the increase of oxygen uptake in sediments. There are two perspective on the role of the oxygen permeable layer in the degradation of organic matter： one is that the oxygen permeable layer is very shallow， so the oxygen-depleting degradation of organic matter cannot occupy an important position. Another is that dissolved oxygen can penetrate deep sediments under the bioturbation， so the degradation of organic matter is not limited to the surface layer of sediments. At present， many experiments have confirmed that bioturbation accelerated the infiltration of dissolved oxygen into sediments and significantly accelerated the degradation of organic matter. Webb and Eyre[7] calculated that 15% of dissolved oxygen in the increased oxygen consumption of sediment by bioturbation was directly consumed by macrobenthos. The rest was used by microorganisms， which significantly accelerated the degradation rate of organic matter. Redox oscillation caused by bioturbation could made organic matter repeatedly exposed to aerobic and anaerobic conditions in the degradation process， so that the mineralization process of organic matter was more rapid. In addition， different disturbance functional groups have different effects on the oxygen consumption rate of sediments. Some studies have shown that gallery-diffusers were more favorable for sediments to absorb oxygen than biodiffusers. Effects on microorganisms in sediments
Bioturbation will affect the microbial community structure in the sediment and activity on the tunnel wall， causing the increase of organic matter utilization in the pipeline， the exacerbation of the fluctuation of chemical reactions and redox conditions. There are more active microorganisms on the surface of the cave wall of many macrobenthos. Nicholaus et al.[8] found that macrobenthos significantly changed the microbial community structure， and believed that bioturbation promoted the mineralization process and created a favorable environment for the proliferation of microbial community. The composition and activity of the microbial community in the cave depend largely on the physical and chemical properties of the cave. These physicochemical characteristics depend on the following factors： ① habitat characteristics， such as organic matter content， particle size distribution， nutrients in water， phytoplankton concentration; ② burrowing macrobenthos ecology， including feeding type， flushing method， migration rate， secretion type; and ③ age and stability of the cave. The microbial community in the sediment determines the trend and net rate of biogeochemical processes， and plays an important role in the conversion of organic matter and the cycle of elements caused by organisms. However， in different cave environments， the reaction rate and community structure of microorganisms are also different， and its potential mechanism is unknown.
Effects on nutrients flux at sediment-water interface
The sediment-water interface is a transition area between water and sediment in the water environment， and it is a special and important area of the water environment. It plays an important role in the circulation， transfer， and storage of water and substrate. The disturbance of macrobenthos can accelerate the mineralization of organic matter in sediments， and enhance the migration of solutes. And bioturbation accelerate the diffusion rate and dissolution rate of substances in pore water. Therefore， the bioturbation could greatly increase the exchange rate of nutrients at the sediment-water interface， so that the nutrients settled in the sediment can be returned to the water body in a few weeks or even less， and be reused. The nitrogen cycle in the sediment occupies an important position in the entire nitrogen cycle system. At present， the study of nitrogen cycle in sediments by bioturbation has been deeply studied in the early diagenesis of nitrogen， nitrification and denitrification of nitrogen， the transfer of nitrogen at the sediment-water interface， and exchange flux. Bioturbation will significantly affect the nitrification and denitrification processes in the sediment， and then affect the nitrogen flux at the sediment-water interface. Most studies believe that bioturbation will promote the release of nitrogen in sediments. Christensen et al.[9] used Nereis diversicolor and N. virens to conducted laboratory tests and found that both can significantly accelerated the release of NH+4 and NO-3 in sediments. Yang et al.[10] studied intensive shrimp ponds and drew similar conclusions that bioturbation promoted the release of NO-2-N， NO-3-N， NH+4-N from the sediments of aquaculture ponds. A large number of studies have shown that bioturbation played an important role in promoting the release of PO3-4-P in sediments， and different benthic animals had different effects on the PO3-4-P flux at the sediment-water interface. Zhang et al.[11-12] found that Tubificid worms and Chironomidae larvae inhibited the release of soluble reactive phosphorus at the sediment-water interface， but Corbicula fluminea promoted the release of soluble reactive phosphorus. Perspectives
The important role and significance of bioturbation in benthic ecosystems and geological evolution have been largely confirmed. The research on the effect of bioturbation started late in China. Since 1980s， many studies on bioturbation have been carried out and fruitful results have been achieved. It is suggested to strengthen the following aspects in the future：
Research method： The relevant research is still focused on the indoor simulation culture experiment， and human interference is inevitable. In the future， we should establish a variety of on-site cultivation systems and strengthen the combination of field experiments and lab simulation test.
Research area： Only in some hot shallow water ecosystems and estuaries （such as Jiaozhou Bay， Yangtze Estuary， etc.） have a relatively complete research foundation of benthic ecology in china， which limits the research area of biological disturbance. In the future， research should be carried out on a wider sea area and different ecosystems （such as coastal wetland ecosystem， rivers， lakes， aquaculture ponds， rice fields， etc.）.
Research content： At present， the research focuses on the effects of macrobenthos on nitrogen， phosphorus and other major biogenic elements. We should strengthen the research on the effects of bioturbation on other biogenic elements， microbial community structure and heavy metals.
Agricultural Biotechnology2020
References
[1] BERNER RA. Early diagenesis： a theoretical approach[M]. 1980， Princeton， New Jersey： Princeton University Press.
[2] LUKWAMBE B， YANG W， ZHENG Y， et al. Bioturbation by the razor clam （Sinonovacula constricta） on the microbial community and enzymatic activities in the sediment of an ecological aquaculture wastewater treatment system[J]. Science of the Total Environment， 2018（643）： 1098-1107.
[3] RHOADS DC. Rates of sediment reworking by Yoldia limatula in Buzzards Bay， Massachusetts， and Long Island Sound[J]. Journal of Sedimentary Research， 1963， 33（3）： 723.
[4] HAVEN DS， MORALES-ALAMO R. Aspects of biodeposition by oysters and other invertebrate filter feeders[J]. Limnology and Oceanography， 1966， 11（4）： 487-498.
[5] JARAMILLO E， BERTRAN C， BRAVO A. Mussel biodeposition in an estuary in southern Chile[J]. Marine ecology progress series， 1992， 82（1）： 85-94.
[6] ZAIKO A， OLENIN S. Impact of invasive benthic crustaceans on the resuspension of bottom sediments： an experimental study approach[J]. Oceanological and Hydrobiological Studies， 2004， 33（3）： 99-110. [7] WEBB AP， EYRE BD. Effect of natural populations of burrowing thalassinidean shrimp on sediment irrigation， benthic metabolism， nutrient fluxes and denitrification[J]. Marine Ecology Progress Series， 2004（268）： 205-220.
[8] NICHOLAUS R， LUKWAMBEA B， ZHAO L， et al. Bioturbation of blood clam Tegillarca granosa on benthic nutrient fluxes and microbial community in an aquaculture wastewater treatment system[J]. International Biodeterioration & Biodegradation， 2019（142）： 73-78.
[9] CHRISTENSEN B， VEDEL A， KRISTENSEN E. Carbon and nitrogen fluxes in sediment inhabited by suspension-feeding （Nereis diversicolor） and non-suspension-feeding （N. virens） polychaetes[J]. Marine Ecology Progress Series， 2000（192）： 203-217.
[10] YANG P， LAI DYF， JIN BS， et al. Dynamics of dissolved nutrients in the aquaculture shrimp ponds of the Min River estuary， China： Concentrations， fluxes and environmental loads[J]. Science of the Total Environment， 2017（603-604）： 256-267.
[11] ZHANGL， GU XZ， FAN CX， et al. Impact of different benthic animals on phosphorus dynamics across the sediment-water interface[J]. Journal of Environmental Sciences， 2010， 22（11）： 1674-1682.
[12] ZHANG L， GU XZ， SHAO SG， et al. Impacts of Asian Clam （Corbicula fluminea） on lake sediment properties and phosphorus movement[J]. Environmental Science， 2011， 32（1）： 88-95.
Key words Organic matter decomposition; Microorganism; Sediment-water interface; Bioturbation
Bioturbation is one of the key ecological processes in estuaries， near shore and shallow waters. Bioturbation refers to the change of solute exchange and particle migration in sediments and sediment-water interface of macrobenthos during their life activities （such as feeding， excretion， burrowing and movement）[1]. The importance of bioturbation was first proposed by Darwin in 1891. A series of subsequent studies confirmed Darwins view and further revealed the important role and significance of bioturbation in benthic ecosystem and geological evolution[2]. However， the bioturbation of macrobenthos and their effects on biogeochemical processes in sediments have not been systematically organized. Thus， the forms of bioturbation and the effects of bioturbation on biogeochemical cycling process in sediments were summarized in order to improve the knowledge system of bioturbation.
Forms of Bioturbation
Rework
Bioturbation fundamentally change the physical and chemical characteristics of sediment， accelerating the material exchange between pore water and overlying water. Thereby， this process affects the stability and erosion rate of sediment， changing the pore rate and surface composition of sediment. Macrobenthos （especially crustaceans） have a strong ability to transform the sediment environment and are called ecosystem engineer. Although these species may not be dominant in number in the community， their strong activity ability， burrowing life habit， and great alteration of sediments can eventually cause fundamental changes in the process of biogeochemistry in sediments. Rhoads[3] observed that a sediment-feeding mollusk （Yoldia Limatula） was able to modify the sediment structure at a rate of up to 50 L/（m2·yr）. Bioirrigation
As a result of respiration or other activities， burrowing macrobenthos can produce rapid water flow in the cave， so that the material diffusion between the overlying water， the deep sediment and pore water can be completed through the cave. This process of material exchange between the overlying water and deep sediment is called bioirrigation. Bioirrigation can transfer dissolved oxygen to deep sediments， thus accelerating the degradation of organic matter. In addition， this process affects the sediment-water interface material exchange.
Biodeposition
Filter-feeding macrobenthos feed on plankton and organic debris in the water layer. In the process of filter feeding， a large number of particles in the water layer are filtered and trapped， and then new sediment is formed in the form of large particles such as feces or pseudofeces. This process is called biological deposition because it speeds up the deposition process of particulate matter in the water layer. Haven and Morales-Alamo[4] calculated that 0.4 hm2 oyster farm in the York estuary could produced 981 kg of feces or pseudofeces per week. In the Queule estuary in Chile， the biodeposition rate of shellfish to organic matter in the water reached 49 g·DW/（m2·d）[5].
Bioresuspension
Macrobenthos produce water flow during burrowing， feeding and excretion， and the process of returning sedimentary particles to the water layer in suspension is called bioresuspension. Zaiko and Olenin[6] verified the possibility of biological resuspension in the laboratory. Bioresuspension is related to the water flow rate at the sediment-water interface. Due to the limitation of research methods， experimental data on bioresuspension are still lacking.
Biodiffusion
Macrobenthos can cause small range of diffusion of sediment and pore water in the process of biological activities， which is called biodiffusion. Experiments have confirmed that the biological activities of different macrobenthos cloud accelerated the diffusion process of sediment particles and pore water. Compared with bioirrigation， however， biodiffusion only involves the short distance migration of materials.
Effects of Bioturbation on the Biogeochemical Cycle in Sediments
Effects on organic matter decomposition
It has been demonstrated that bioturbation promoted the increase of oxygen uptake in sediments. There are two perspective on the role of the oxygen permeable layer in the degradation of organic matter： one is that the oxygen permeable layer is very shallow， so the oxygen-depleting degradation of organic matter cannot occupy an important position. Another is that dissolved oxygen can penetrate deep sediments under the bioturbation， so the degradation of organic matter is not limited to the surface layer of sediments. At present， many experiments have confirmed that bioturbation accelerated the infiltration of dissolved oxygen into sediments and significantly accelerated the degradation of organic matter. Webb and Eyre[7] calculated that 15% of dissolved oxygen in the increased oxygen consumption of sediment by bioturbation was directly consumed by macrobenthos. The rest was used by microorganisms， which significantly accelerated the degradation rate of organic matter. Redox oscillation caused by bioturbation could made organic matter repeatedly exposed to aerobic and anaerobic conditions in the degradation process， so that the mineralization process of organic matter was more rapid. In addition， different disturbance functional groups have different effects on the oxygen consumption rate of sediments. Some studies have shown that gallery-diffusers were more favorable for sediments to absorb oxygen than biodiffusers. Effects on microorganisms in sediments
Bioturbation will affect the microbial community structure in the sediment and activity on the tunnel wall， causing the increase of organic matter utilization in the pipeline， the exacerbation of the fluctuation of chemical reactions and redox conditions. There are more active microorganisms on the surface of the cave wall of many macrobenthos. Nicholaus et al.[8] found that macrobenthos significantly changed the microbial community structure， and believed that bioturbation promoted the mineralization process and created a favorable environment for the proliferation of microbial community. The composition and activity of the microbial community in the cave depend largely on the physical and chemical properties of the cave. These physicochemical characteristics depend on the following factors： ① habitat characteristics， such as organic matter content， particle size distribution， nutrients in water， phytoplankton concentration; ② burrowing macrobenthos ecology， including feeding type， flushing method， migration rate， secretion type; and ③ age and stability of the cave. The microbial community in the sediment determines the trend and net rate of biogeochemical processes， and plays an important role in the conversion of organic matter and the cycle of elements caused by organisms. However， in different cave environments， the reaction rate and community structure of microorganisms are also different， and its potential mechanism is unknown.
Effects on nutrients flux at sediment-water interface
The sediment-water interface is a transition area between water and sediment in the water environment， and it is a special and important area of the water environment. It plays an important role in the circulation， transfer， and storage of water and substrate. The disturbance of macrobenthos can accelerate the mineralization of organic matter in sediments， and enhance the migration of solutes. And bioturbation accelerate the diffusion rate and dissolution rate of substances in pore water. Therefore， the bioturbation could greatly increase the exchange rate of nutrients at the sediment-water interface， so that the nutrients settled in the sediment can be returned to the water body in a few weeks or even less， and be reused. The nitrogen cycle in the sediment occupies an important position in the entire nitrogen cycle system. At present， the study of nitrogen cycle in sediments by bioturbation has been deeply studied in the early diagenesis of nitrogen， nitrification and denitrification of nitrogen， the transfer of nitrogen at the sediment-water interface， and exchange flux. Bioturbation will significantly affect the nitrification and denitrification processes in the sediment， and then affect the nitrogen flux at the sediment-water interface. Most studies believe that bioturbation will promote the release of nitrogen in sediments. Christensen et al.[9] used Nereis diversicolor and N. virens to conducted laboratory tests and found that both can significantly accelerated the release of NH+4 and NO-3 in sediments. Yang et al.[10] studied intensive shrimp ponds and drew similar conclusions that bioturbation promoted the release of NO-2-N， NO-3-N， NH+4-N from the sediments of aquaculture ponds. A large number of studies have shown that bioturbation played an important role in promoting the release of PO3-4-P in sediments， and different benthic animals had different effects on the PO3-4-P flux at the sediment-water interface. Zhang et al.[11-12] found that Tubificid worms and Chironomidae larvae inhibited the release of soluble reactive phosphorus at the sediment-water interface， but Corbicula fluminea promoted the release of soluble reactive phosphorus. Perspectives
The important role and significance of bioturbation in benthic ecosystems and geological evolution have been largely confirmed. The research on the effect of bioturbation started late in China. Since 1980s， many studies on bioturbation have been carried out and fruitful results have been achieved. It is suggested to strengthen the following aspects in the future：
Research method： The relevant research is still focused on the indoor simulation culture experiment， and human interference is inevitable. In the future， we should establish a variety of on-site cultivation systems and strengthen the combination of field experiments and lab simulation test.
Research area： Only in some hot shallow water ecosystems and estuaries （such as Jiaozhou Bay， Yangtze Estuary， etc.） have a relatively complete research foundation of benthic ecology in china， which limits the research area of biological disturbance. In the future， research should be carried out on a wider sea area and different ecosystems （such as coastal wetland ecosystem， rivers， lakes， aquaculture ponds， rice fields， etc.）.
Research content： At present， the research focuses on the effects of macrobenthos on nitrogen， phosphorus and other major biogenic elements. We should strengthen the research on the effects of bioturbation on other biogenic elements， microbial community structure and heavy metals.
Agricultural Biotechnology2020
References
[1] BERNER RA. Early diagenesis： a theoretical approach[M]. 1980， Princeton， New Jersey： Princeton University Press.
[2] LUKWAMBE B， YANG W， ZHENG Y， et al. Bioturbation by the razor clam （Sinonovacula constricta） on the microbial community and enzymatic activities in the sediment of an ecological aquaculture wastewater treatment system[J]. Science of the Total Environment， 2018（643）： 1098-1107.
[3] RHOADS DC. Rates of sediment reworking by Yoldia limatula in Buzzards Bay， Massachusetts， and Long Island Sound[J]. Journal of Sedimentary Research， 1963， 33（3）： 723.
[4] HAVEN DS， MORALES-ALAMO R. Aspects of biodeposition by oysters and other invertebrate filter feeders[J]. Limnology and Oceanography， 1966， 11（4）： 487-498.
[5] JARAMILLO E， BERTRAN C， BRAVO A. Mussel biodeposition in an estuary in southern Chile[J]. Marine ecology progress series， 1992， 82（1）： 85-94.
[6] ZAIKO A， OLENIN S. Impact of invasive benthic crustaceans on the resuspension of bottom sediments： an experimental study approach[J]. Oceanological and Hydrobiological Studies， 2004， 33（3）： 99-110. [7] WEBB AP， EYRE BD. Effect of natural populations of burrowing thalassinidean shrimp on sediment irrigation， benthic metabolism， nutrient fluxes and denitrification[J]. Marine Ecology Progress Series， 2004（268）： 205-220.
[8] NICHOLAUS R， LUKWAMBEA B， ZHAO L， et al. Bioturbation of blood clam Tegillarca granosa on benthic nutrient fluxes and microbial community in an aquaculture wastewater treatment system[J]. International Biodeterioration & Biodegradation， 2019（142）： 73-78.
[9] CHRISTENSEN B， VEDEL A， KRISTENSEN E. Carbon and nitrogen fluxes in sediment inhabited by suspension-feeding （Nereis diversicolor） and non-suspension-feeding （N. virens） polychaetes[J]. Marine Ecology Progress Series， 2000（192）： 203-217.
[10] YANG P， LAI DYF， JIN BS， et al. Dynamics of dissolved nutrients in the aquaculture shrimp ponds of the Min River estuary， China： Concentrations， fluxes and environmental loads[J]. Science of the Total Environment， 2017（603-604）： 256-267.
[11] ZHANGL， GU XZ， FAN CX， et al. Impact of different benthic animals on phosphorus dynamics across the sediment-water interface[J]. Journal of Environmental Sciences， 2010， 22（11）： 1674-1682.
[12] ZHANG L， GU XZ， SHAO SG， et al. Impacts of Asian Clam （Corbicula fluminea） on lake sediment properties and phosphorus movement[J]. Environmental Science， 2011， 32（1）： 88-95.