Bioturbation


Bioturbation is defined as the reworking of soils and sediments by animals or plants. It includes burrowing, ingestion, and defecation of sediment grains. Bioturbating activities have a profound effect on the environment and are thought to be a primary driver of biodiversity. The formal study of bioturbation began in the 1800s by Charles Darwin experimenting in his garden. The disruption of aquatic sediments and terrestrial soils through bioturbating activities provides significant ecosystem services. These include the alteration of nutrients in aquatic sediment and overlying water, shelter to other species in the form of burrows in terrestrial and water ecosystems, and soil production on land.
Bioturbators are deemed ecosystem engineers because they alter resource availability to other species through the physical changes they make to their environments. This type of ecosystem change affects the evolution of cohabitating species and the environment, which is evident in trace fossils left in marine and terrestrial sediments. Other bioturbation effects include altering the texture of sediments, 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.
Walruses, salmon, and pocket gophers are examples of large bioturbators. Although the activities of these large macrofaunal bioturbators are more conspicuous, the dominant bioturbators are small invertebrates, such as earthworms, polychaetes, ghost shrimp, mud shrimp, and midge larvae. The activities of these small invertebrates, which include burrowing and ingestion and defecation of sediment grains, contribute to mixing and the alteration of sediment structure.

Functional groups

Bioturbators have been organized by a variety of functional groupings based on either ecological characteristics or biogeochemical effects. 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 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, feeding and biological interactions, and mobility modes. 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. Gallery-diffusers are heavily associated with burrowing polychaetes, such as Nereis diversicolor and Marenzelleria spp.
  • Biodiffusers transport sediment particles randomly over short distances as they move through sediments. Animals mostly attributed to this category include bivalves such as clams, and amphipod species, but can also include larger vertebrates, such as bottom-dwelling fish and rays that feed along the sea floor. Biodiffusers can be further divided into two subgroups, which include epifaunal biodiffusers and surface biodiffusers. This subgrouping may also include gallery-diffusers, 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. Major upward-conveyor groups include burrowing polychaetes like the lugworm, Arenicola marina, and thalassinid shrimps.
  • Downward-conveyor species are oriented with their heads towards the sediment-water interface and defecation occurs at depth. Their activities transport sediment from the surface to deeper sediment layers as they feed. Notable downward-conveyors include those in the peanut worm family, Sipunculidae.
  • Regenerators are categorized by their ability to release sediment to the overlying water column, which is then dispersed as they burrow. After regenerators abandon their burrows, water flow at the sediment surface can push in and collapse the burrow. Examples of regenerator species include fiddler and ghost crabs.

    Ecological roles

The evaluation of the ecological role of bioturbators has largely been species-specific. 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.
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. 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. This increase in sediment metabolism and microbial activity further results in enhanced organic matter decomposition and sediment oxygen uptake. 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. This increased microbial activity by bioturbators can contribute to increased nutrient release to the overlying water column. 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.
Burrows offer protection from predation and harsh environmental conditions. For example, termites burrow and create mounds that have a complex system of air ducts and evaporation devices that create a suitable microclimate in an unfavorable physical environment. Many species are attracted to bioturbator burrows because of their protective capabilities. The shared use of burrows has enabled the evolution of symbiotic relationships between bioturbators and the many species that utilize their burrows. For example, gobies, scale-worms, and crabs live in the burrows made by innkeeper worms. Social interactions provide evidence of co-evolution between hosts and their burrow symbionts. This is exemplified by shrimp-goby associations. Shrimp burrows provide shelter for gobies and gobies serve as a scout at the mouth of the burrow, signaling the presence of potential danger. In contrast, the blind goby Typhlogobius californiensis lives within the deep portion of Callianassa shrimp burrows where there is not much light. The blind goby is an example of a species that is an obligate commensalist, meaning their existence depends on the host bioturbator and its burrow. Although newly hatched blind gobies have fully developed eyes, their eyes become withdrawn and covered by skin as they develop. They show evidence of commensal morphological evolution because it is hypothesized that the lack of light in the burrows where the blind gobies reside is responsible for the evolutionary loss of functional eyes.
Bioturbators can also inhibit the presence of other benthic organisms by smothering, exposing other organisms to predators, or resource competition. While thalassinidean shrimps can provide shelter for some organisms and cultivate interspecies relationships within burrows, they have also been shown to have strong negative effects on other species, especially those of bivalves and surface-grazing gastropods, because thalassinidean shrimps can smother bivalves when they resuspend sediment. They have also been shown to exclude or inhibit polychaetes, cumaceans, and amphipods. This has become a serious issue in the northwestern United States, as ghost and mud shrimp are considered pests to bivalve aquaculture operations. The presence of bioturbators can have both negative and positive effects on the recruitment of larvae of conspecifics and those of other species, as the resuspension of sediments and alteration of flow at the sediment-water interface can affect the ability of larvae to burrow and remain in sediments. This effect is largely species-specific, as species differences in resuspension and burrowing modes have variable effects on fluid dynamics at the sediment-water interface. Deposit-feeding bioturbators may also hamper recruitment by consuming recently settled larvae.

Biogeochemical effects

Since its onset around 539 million years ago, bioturbation has been responsible for changes in ocean chemistry, primarily through nutrient cycling. Bioturbators played, and continue to play, an important role in nutrient transport across sediments.
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, animals begin to mix reduced sulfur from ocean sediments to overlying water causing sulfide to oxidize, which increased the sulfate composition in the ocean. During large extinction events, the sulfate concentration in the ocean was reduced. Although this is difficult to measure directly, seawater sulfur isotope compositions during these times indicates bioturbators influenced the sulfur cycling in the early Earth.
Bioturbators have also altered phosphorus cycling on geologic scales. Bioturbators mix readily available particulate organic phosphorus deeper into ocean sediment layers which prevents the precipitation of phosphorus by increasing the sequestration of phosphorus above normal chemical rates. The sequestration of phosphorus limits oxygen concentrations by decreasing production on a geologic time scale. This decrease in production results in an overall decrease in oxygen levels, and it has been proposed that the rise of bioturbation corresponds to a decrease in oxygen levels of that time. The negative feedback of animals sequestering phosphorus in the sediments and subsequently reducing oxygen concentrations in the environment limits the intensity of bioturbation in this early environment.