Benthic macroinvertebrate functional diversity regulates nutrient and algal dynamics in a shallow estuary

Abstract

Proliferation of macroalgal blooms is regulated by grazing pressure and nutrient availability, which may be mediated directly by benthic macroinvertebrates or indirectly through feedback mechanisms. Using invertebrates common to a shallow estuary in Cape Cod, Massachusetts (USA), we determined effects of faunal diversity on benthic microalgae, net ecosystem metabolism, sediment nutrient fluxes, and macroalgal biomass and productivity. Laboratory microcosms contained sediments with single-and mixed-species invertebrate assemblages, in the presence of (1) no macroalgae, (2) a macroalgal monoculture, and (3) a realistic macroalgal polyculture. The depositfeeding gastropod Ilyanassa obsoleta suppressed benthic microalgae, enhanced nitrate efflux from sediments, and maintained macroalgal standing stocks. Conversely, the burrowing, omnivorous polychaete Alitta (formerly Nereis) virens stimulated benthic microalgal growth, inhibited efflux of ammonium, and drastically reduced macroalgal biomass via grazing and translocation of thalli below the sediment surface. In the polyculture experiment, A. virens sequentially removed Gracilaria sp. (Rhodophyta), Ulva sp. (Chlorophyta), and finally Fucus vesiculosus (Phaeophyta). The bivalve Mya arenaria exhibited limited effects on benthic dynamics. In mixed-fauna assemblages, biomass and productivity of benthic microalgae and macroalgae were consistently lower than predicted, revealing non-additive effects of biodiversity. Communities dominated by I. obsoleta or other surficial grazers could indirectly promote macroalgal blooms via sustained release of sediment-derived nutrients and reduction of benthic microalgae. In contrast, omnivorous burrowers such as A. virens may buffer symptoms of eutrophication through inhibition of ammonium supply and direct grazing of bloomforming macroalgae. Overall, our results highlight species-specific effects on key ecosystem functions, and demonstrate important feedbacks between top-down and bottom-up controls in shallow estuaries.

Nuevas perspectivas en la diversidad funcional de ambientes marinos

“…En ambientes acuáticos la mayor cantidad de trabajos relacionados con la diversidad funcional se ha desarrollado en macro-invertebrados riparios (Heino, 2005(Heino, , 2008Heino et al, 2007 con el enfoque hacia el análisis de los atributos funcionales), así como en zonas costeras de sustrato rocoso (Crowe & Russel, 2009;Clemente et al, 2010), fondos blandos (Pacheco et al, 2011) y estuarios (Villéger et al, 2008McLenaghan et al, 2011).…”

Do snails facilitate bloom-forming macroalgae in a eutrophic estuary?

“…High densities of some macroinvertebrates have been observed in association with bloom forming macroalgae (Fong et al, 1997;Guidone et al, 2010), and it has been recently suggested that these numerous herbivores may be facilitating blooms rather than simply opportunistically grazing on the abundant macroalgal biomass (Guidone et al, 2010(Guidone et al, , 2012McLenaghan et al, 2011). There is a body of research that suggests herbivore facilitation of macroalgal blooms might be possible since grazers can have the paradoxical effect of enhancing growth of macroalgae under equilibrium (non-bloom) conditions by three possible mechanisms.…”

“…Second, herbivores may facilitate macroalgae by selectively grazing on the epiphytes that would otherwise compete with macroalgae for nutrients and light (Duffy, 1990;Guidone et al, 2010;Raberg and Kautsky, 2008). Finally, in soft-bottomed environments, surface depositfeeding gastropods can impact nutrient cycling, benthic microalgae, and oxygenation of surface sediment (Ieno et al, 2006;McLenaghan et al, 2011;Pillay et al, 2009;Premo, 2011;Weerman et al, 2011). By removing benthic microalgae, "bull-dozing" sediments, or otherwise altering the redox status at the sediment surface, snails can promote benthic-pelagic coupling by increasing the efflux of N mineralized in the sediments to the water column where it is presumably available for uptake by macroalgae (Ieno et al, 2006;McLenaghan et al, 2011;Raffaelli, 2006).…”

“…Finally, in soft-bottomed environments, surface depositfeeding gastropods can impact nutrient cycling, benthic microalgae, and oxygenation of surface sediment (Ieno et al, 2006;McLenaghan et al, 2011;Pillay et al, 2009;Premo, 2011;Weerman et al, 2011). By removing benthic microalgae, "bull-dozing" sediments, or otherwise altering the redox status at the sediment surface, snails can promote benthic-pelagic coupling by increasing the efflux of N mineralized in the sediments to the water column where it is presumably available for uptake by macroalgae (Ieno et al, 2006;McLenaghan et al, 2011;Raffaelli, 2006). If snails did enhance macroalgal blooms by one of these mechanisms, as suggested, it would have broad implications for nutrient retention and cycling in estuaries.…”

Multi-decadal changes in two co-occurring ophiuroid populations

“…Sediment reworking through ophiuroid bioturbation also contributes to sediment biochemical processes (Lohrer et al 2004, Webb & Eyre 2004, McLenaghan et al 2011. Because of its high densities and its mobility and burrowing activity within the superficial sediment layers, Ophiocomina nigra is likely to locally affect nutrient cycling at the sediment surface and ultimately modify the associated benthic assemblages.…”