Bioturbation
Bioturbation is defined as the reworking of
Bioturbators are deemed ecosystem engineers because they alter resource availability to other species through the physical changes they make to their environments.[5] This type of ecosystem change affects the evolution of cohabitating species and the environment,[5] which is evident in trace fossils left in marine and terrestrial sediments. Other bioturbation effects include altering the texture of sediments (diagenesis), bioirrigation, and displacement of microorganisms and non-living particles. Bioturbation is sometimes confused with the process of bioirrigation, however these processes differ in what they are mixing; bioirrigation refers to the mixing of water and solutes in sediments and is an effect of bioturbation.[3]
Functional groups
Bioturbators have been organized by a variety of functional groupings based on either ecological characteristics or biogeochemical effects.[9][10] While the prevailing categorization is based on the way bioturbators transport and interact with sediments, the various groupings likely stem from the relevance of a categorization mode to a field of study (such as ecology or sediment biogeochemistry) and an attempt to concisely organize the wide variety of bioturbating organisms in classes that describe their function. Examples of categorizations include those based on feeding and motility,[11] feeding and biological interactions,[12] and mobility modes.[13] The most common set of groupings are based on sediment transport and are as follows:
- Gallery-diffusers create complex tube networks within the upper sediment layers and transport sediment through feeding, burrow construction, and general movement throughout their galleries.
- Biodiffusers transport sediment particles randomly over short distances as they move through sediments. Animals mostly attributed to this category include reducing the number of functional groups.
- Upward-conveyors are oriented head-down in sediments, where they feed at depth and transport sediment through their guts to the sediment surface.
- Downward-conveyor species are oriented with their heads towards the sediment-water interface and defecation occurs at depth.[14] Their activities transport sediment from the surface to deeper sediment layers as they feed.[14] Notable downward-conveyors include those in the peanut worm family, Sipunculidae.[14]
- Regenerators are categorized by their ability to release sediment to the overlying water column, which is then dispersed as they burrow.[14] After regenerators abandon their burrows, water flow at the sediment surface can push in and collapse the burrow.[5][14] Examples of regenerator species include fiddler and ghost crabs.[5]
Ecological roles
The evaluation of the ecological role of bioturbators has largely been species-specific.[8] However, their ability to transport solutes, such as dissolved oxygen, enhance organic matter decomposition and diagenesis, and alter sediment structure has made them important for the survival and colonization by other macrofaunal and microbial communities.[8]
Microbial communities are greatly influenced by bioturbator activities, as increased transport of more energetically favorable oxidants, such as oxygen, to typically highly reduced sediments at depth alters the microbial metabolic processes occurring around burrows.[17][15] As bioturbators burrow, they also increase the surface area of sediments across which oxidized and reduced solutes can be exchanged, thereby increasing the overall sediment metabolism.[18] This increase in sediment metabolism and microbial activity further results in enhanced organic matter decomposition and sediment oxygen uptake.[15] In addition to the effects of burrowing activity on microbial communities, studies suggest that bioturbator fecal matter provides a highly nutritious food source for microbes and other macrofauna, thus enhancing benthic microbial activity.[15] This increased microbial activity by bioturbators can contribute to increased nutrient release to the overlying water column.[19] Nutrients released from enhanced microbial decomposition of organic matter, notably limiting nutrients, such as ammonium, can have bottom-up effects on ecosystems and result in increased growth of phytoplankton and bacterioplankton.[19][20][21]
Burrows offer protection from predation and harsh environmental conditions.
Bioturbators can also inhibit the presence of other benthic organisms by smothering, exposing other organisms to predators, or resource competition.
Biogeochemical effects
Since its onset around 539 million years ago, bioturbation has been responsible for changes in
For example, bioturbating animals are hypothesized to have affected the cycling of sulfur in the early oceans. According to this hypothesis, bioturbating activities had a large effect on the sulfate concentration in the ocean. Around the Cambrian-Precambrian boundary (539 million years ago), animals begin to mix reduced sulfur from
Bioturbators have also altered phosphorus cycling on geologic scales.
Organic contaminants
Bioturbation can either enhance or reduce the
Ecosystem impacts
Terrestrial
Plants and animals utilize soil for food and shelter, disturbing the upper soil layers and transporting chemically weathered rock called
Freshwater
Important sources of bioturbation in freshwater ecosystems include benthivorous (bottom-dwelling) fish, macroinvertebrates such as worms, insect larvae, crustaceans and molluscs, and seasonal influences from anadromous (migrating) fish such as salmon. Anadromous fish migrate from the sea into fresh-water rivers and streams to spawn. Macroinvertebrates act as biological pumps for moving material between the sediments and water column, feeding on sediment organic matter and transporting mineralized nutrients into the water column.[42] Both benthivorous and anadromous fish can affect ecosystems by decreasing primary production through sediment re-suspension,[42] the subsequent displacement of benthic primary producers, and recycling nutrients from the sediment back into the water column.[43][44]
Lakes and ponds
The sediments of lake and pond ecosystems are rich in organic matter, with higher organic matter and nutrient contents in the sediments than in the overlying water.
Lake and pond sediments often transition from the aerobic (oxygen containing) character of the overlaying water to the anaerobic (without oxygen) conditions of the lower sediment over sediment depths of only a few millimeters, therefore, even bioturbators of modest size can affect this transition of the chemical characteristics of sediments.[42] By mixing anaerobic sediments into the water column, bioturbators allow aerobic processes to interact with the re-suspended sediments and the newly exposed bottom sediment surfaces.[42]
Macroinvertebrates including chironomid (non-biting midges) larvae and tubificid worms (detritus worms) are important agents of bioturbation in these ecosystems and have different effects based on their respective feeding habits. Tubificid worms do not form burrows, they are upward conveyors. Chironomids, on the other hand, form burrows in the sediment, acting as bioirrigators and aerating the sediments and are downward conveyors. This activity, combined with chironomid's respiration within their burrows, decrease available oxygen in the sediment and increase the loss of nitrates through enhanced rates of denitrification.[42]
The increased oxygen input to sediments by macroinvertebrate bioirrigation coupled with bioturbation at the sediment-water interface complicates the total flux of phosphorus . While bioturbation results in a net flux of phosphorus into the water column, the bio-irrigation of the sediments with oxygenated water enhances the adsorption of phosphorus onto iron-oxide compounds, thereby reducing the total flux of phosphorus into the water column.[42]
The presence of macroinvertebrates in sediment can initiate bioturbation due to their status as an important food source for benthivorous fish such as
Rivers and streams
River and stream ecosystems show similar responses to bioturbation activities, with chironomid larvae and tubificid worm macroinvertebrates remaining as important benthic agents of bioturbation.[45] These environments can also be subject to strong season bioturbation effects from anadromous fish.[46]
The construction of salmon redds increases sediment and nutrient fluxes through the hyporheic zone (area between surface water and groundwater) of rivers and effects the dispersion and retention of marine derived nutrients (MDN) within the river ecosystem.[47] MDN are delivered to river and stream ecosystems by the fecal matter of spawning salmon and the decaying carcasses of salmon that have completed spawning and died.[47] Numerical modeling suggests that residence time of MDN within a salmon spawning reach is inversely proportional to the amount of redd construction within the river.[47] Measurements of respiration within a salmon-bearing river in Alaska further suggest that salmon bioturbation of the river bed plays a significant role in mobilizing MDN and limiting primary productivity while salmon spawning is active.[44] The river ecosystem was found to switch from a net autotrophic to heterotrophic system in response to decreased primary production and increased respiration.[44] The decreased primary production in this study was attributed to the loss of benthic primary producers who were dislodged due to bioturbation, while increased respiration was thought to be due to increased respiration of organic carbon, also attributed to sediment mobilization from salmon redd construction.[44] While marine derived nutrients are generally thought to increase productivity in riparian and freshwater ecosystems, several studies have suggested that temporal effects of bioturbation should be considered when characterizing salmon influences on nutrient cycles.[44][47]
Marine
Major marine bioturbators range from small
Shallow and coastal
The effects of bioturbation on the nitrogen cycle are well-documented.
Bioturbation by walrus feeding is a significant source of sediment and biological community structure and nutrient flux in the Bering Sea.[1] Walruses feed by digging their muzzles into the sediment and extracting clams through powerful suction.[1] By digging through the sediment, walruses rapidly release large amounts of organic material and nutrients, especially ammonium, from the sediment to the water column.[1] Additionally, walrus feeding behavior mixes and oxygenates the sediment and creates pits in the sediment which serve as new habitat structures for invertebrate larvae.[1]
Deep sea
Bioturbation is important in the deep sea because
Mathematical modelling
The role of bioturbators in sediment biogeochemistry makes bioturbation a common parameter in sediment biogeochemical models, which are often
Parameterization of bioturbation, however, can vary, as newer and more complex models can be used to fit tracer profiles. Unlike the standard biodiffusion model, these more complex models, such as expanded versions of the biodiffusion model, random walk, and particle-tracking models, can provide more accuracy, incorporate different modes of sediment transport, and account for more spatial heterogeneity.[63][64][65][66]
Evolution
The onset of bioturbation had a profound effect on the environment and the evolution of other organisms.
An alternate, less widely accepted hypothesis for the origin of bioturbation exists. The trace fossil Nenoxites is thought to be the earliest record of bioturbation, predating the Cambrian Period.[67] The fossil is dated to 555 million years, which places it in the Ediacaran Period.[67] The fossil indicates a 5 centimeter depth of bioturbation in muddy sediments by a burrowing worm.[67] This is consistent with food-seeking behavior, as there tended to be more food resources in the mud than the water column.[68] However, this hypothesis requires more precise geological dating to rule out an early Cambrian origin for this specimen.[69]
The evolution of trees during the Devonian Period enhanced soil weathering and increased the spread of soil due to bioturbation by tree roots.[70] Root penetration and uprooting also enhanced soil carbon storage by enabling mineral weathering and the burial of organic matter.[70]
Fossil record
Patterns or traces of bioturbation are preserved in
Important
Research history
Bioturbation's importance for soil processes and
See also
References
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