Ecosystem engineering: the impact of bioturbation on biogeochemical processes in marine and freshwater benthic habitats

Abstract

In aquatic ecosystems, invertebrate bioturbation signifi cantly infl uences microbial activities and biogeochemical processes in sediments by modifying water and sediment fl uxes at the water-sediment interface. We apply the concept of ecosystem engineering to develop a qualitative general understanding of the role of bioturbation on microbial processes in different benthic environments. We hypothesized that the effects of the bioturbation mode (sediment reworking, biogenic structure building, bioirrigation) on microbial processes vary between diffusion-and advection-dominated benthic environments because bioturbation does not have the same infl uences on hydrological exchanges (and the fl ux of resources for micro-organisms living in sediments) at the water-sediment interface of the two systems. To test this hypothesis, we experimentally compared the infl uence of three bioturbation modes (fi ne-sediment reworking, U-shaped structure burrowing, and gallery-network burrowing) in a diffusion-dominated system (fi ne sediments/low interstitial fl ow rates) and an advectiondominated system (coarse sediments/advection of water in sediments). Our analysis demonstrated that bioturbation modes in the two systems had different impacts on microbial activities. For instance, U-shaped tube burrowing by animals increased O 2 consumption in the diffusion-dominated system but produced the opposite effect in the advection-dominated system. The infl uence of bioturbation was also negatively related to interstitial fl ow rate, the bioturbation having a higher infl uence on O 2 consumption in the diffusion-dominated system than in the advection-dominated system. According to our hypothesis, bioturbation modifi ed microbial processes in sediments depend on the hydrological characteristics of the system. In the diffusion-dominated system, invertebrate bioturbation can produce water fl uxes at the watersediment interface that may strongly infl uence microbial processes in sediments. In contrast, in the advectiondominated system, invertebrate bioturbation can only modify the water circulation patterns in sediments, moderately affecting microbial processes. Consequently, it is necessary to use a conceptual framework which takes into account the features of sediment habitats in order to allow a better prediction of bioturbation effects on sediment biogeochemistry. With this aim, the conceptual scheme of ecosystem engineers can be an organizing principle to integrate the complex relationships among physical habitat, bioturbation mode and microbial activity.

Decoupling of body-plan diversification and ecological structuring during the Ediacaran–Cambrian transition: evolutionary and geobiological feedbacks

“…The first event involves the appearance of a wide repertoire of behavioural strategies reflecting the interactions of newly developed, distinctive body plans with the substrate. Most of these interactions were characterized by the reworking of fine-grained sediments by sediment bulldozers in diffusion-dominated benthic systems [41], as typified by bioturbation in offshore deposits. This style of biogenic reworking was probably conducive to large-scale changes in both the sediment and the water column, including promotion of water fluxes at the sediment -water interface, average deepening of the redox discontinuity surface, release of nitrogen from the sediment, increase in the sedimentwater flux of iron and manganese, and several-fold increase in seawater sulfate concentration [41,42].…”

“…Most of these interactions were characterized by the reworking of fine-grained sediments by sediment bulldozers in diffusion-dominated benthic systems [41], as typified by bioturbation in offshore deposits. This style of biogenic reworking was probably conducive to large-scale changes in both the sediment and the water column, including promotion of water fluxes at the sediment -water interface, average deepening of the redox discontinuity surface, release of nitrogen from the sediment, increase in the sedimentwater flux of iron and manganese, and several-fold increase in seawater sulfate concentration [41,42]. By being the primary determinant of oxygen concentration in the sediment, bioturbation may have also influenced the biomass of organisms, the expansion of aerobic bacteria, the rate of organic matter decomposition and the regeneration of nutrients vital for primary productivity, among other aspects [43][44][45].…”

Benthic fluxes of oxygen and nutrients in sublittoral fine sands in a north-western Mediterranean coastal area

“…On the one hand, bioturbators change sediment properties by their activity in sediment affecting the redox conditions and increasing DO supply to deeper layers (Mermillod-Blondin and Rosenberg, 2006). On the other hand, in the lining of burrows generated by macrofauna and their faecal pellets there are favourable conditions for microbial activity and nitrification (Blackburn and Henriksen., 1983;Henriksen et al, 1983;Kristensen et al, 1985).…”

“…Many authors, such as Loassachan et al (2009), Mermillod-Blondin et al (2008), and Sarker et al (2009), have described the large number of factors that regulate the availability and regeneration of nutrients in inner shelve bottoms. The main factors are microbial community (Jørgensen, 2006), benthic macrofauna (Mermillod-Blondin and Rosenberg, 2006), quantity and quality of organic matter (Pastor et al, 2011) and benthic primary producers (Mermillod-Blondin et al, 2008) such as seagrasses, macroalgae, as well as microalgae, although a great number of environmental ones, such as temperature or light, can affect all of these.…”

Mediation of nitrogen by post-disturbance shelf communities experiencing organic matter enrichment

“…To widen the generalizability of our conclusions, we examine the effects of chronic fishing disturbance and organic matter enrichment on nitrogen cycling in different sediment types; a diffusion dominated community (sandy mud) and an advection dominated community (sand). We assume that the level of biogeochemical performance that is realized in either sediment type will depend at least in part on the structure and composition of the post-disturbance macro-invertebrate community, as the active redistribution of particles and fluids by the macrofauna disproportionately influences benthic fluxes and total benthic metabolism (Mermillod-Blondin et al 2004;Mermillod-Blondin and Rosenberg 2006).…”