Massive silicon utilization facilitated by a benthic‐pelagic coupled feedback sustains deep‐sea sponge aggregations

Abstract

Biogeochemical cycling of silicon (Si), largely affected by biological drivers, is pivotal to the ecological functioning of the ocean. Most knowledge regarding biological utilization of Si derives from research on phototrophic organisms circumscribed to the photic ocean (i.e., diatoms). Utilization of Si in the aphotic ocean, where heterotrophic silicifiers become relevant Si users, remains poorly investigated. Here we quantify the flux rates and stocks characterizing Si cycling across dense aggregations of the hexactinellid sponge Vazella pourtalesii established in the aphotic zone of the central Scotian Shelf, Nova Scotia, Canada. Although individual rates of silicic acid consumption were low compared to other sponge species and diatoms, the large abundance of individuals (6.5 million) over the extension of these sponge grounds (2105 km 2) leads to massive annual silicic acid consumption, invested in producing their siliceous skeletons of biogenic silica. This sponge activity accumulates large biogenic silica stocks both in the living population and in the sediments. Skeletal pieces in sediment revealed that a good portion of biogenic silica deposited to the bottom after sponge death recycles as silicic acid before being permanently buried. This biogenic silica-silicic acid turnover, facilitated by an unconventional silicification pattern that favors delamination and dissolution of V. pourtalesii spicules, causes silicic acid enrichment at oceanographic dimensions in the bottom water of the central Scotian Shelf. Silicic acid efflux from the bottom sustains a feedback mechanism that fulfills sponge needs for silicic acid and facilitates the persistence of sponge aggregations in the long term. Silicon (Si), in the form of soluble silicic acid, is a key inorganic nutrient in the ocean. Its availability modulates ocean primary productivity (Nelson et al. 1995; Tréguer et al. 1995) and the CO 2 exchange with the atmosphere (Mackenzie and Garrels 1966; Tréguer and Pondaven 2000). Regional patterns of silicic acid availability largely result from

Seasonal Variability in Near-bed Environmental Conditions in the Vazella pourtalesii Glass Sponge Grounds of the Scotian Shelf

“…Accumulations of dead individuals have been observed in the Sambro Bank Sponge Conservation Area (Hawkes et al, 2019), caused either by the displacement by high currents or by fishing activities and subsequent transport by the current (trawling and dumping). Our video data showed that large dead individuals were disintegrating in a period of several weeks, which might be important for the silicon cycling on the Scotian Shelf (Maldonado et al, 2020).…”

“…This species is distributed along the continental margin of eastern North America, from the Florida Keys in the southern US, where it occurs in low densities, to the Scotian Shelf, where it forms extensive monospecific aggregations between ∼150 and 240 m depth in The Emerald Basin, reaching average densities of 3.8 ind. m −2 (Hawkes et al, 2019;Maldonado et al, 2020). Single individuals were found in an even broader depth range between ∼100 to 498 m depth on the Scotian Shelf (Beazley et al, 2018).…”

“…Furthermore, they can release particulate detritus to the associated benthic environment (Reiswig, 1971), a pathway referred to as the sponge loop (Rix et al, 2016). Consequently they transfer energy and nutrients from the pelagic to the benthic environment, and play an important role in carbon, nitrogen, phosphate and silicon cycling (Maldonado et al, 2012;Kutti et al, 2013;Cathalot et al, 2015;Maldonado et al, 2020).…”

Reproductive Biology of Geodia Species (Porifera, Tetractinellida) From Boreo-Arctic North-Atlantic Deep-Sea Sponge Grounds

“…These habitats are formed by three-dimensional structures created by the sponges, which provide refuge for other animals, sometimes of high economic value, and enhance biodiversity (e.g., Klitgaard, 1995;Beazley et al, 2013Beazley et al, , 2015Kenchington et al, 2013). Furthermore, because of their high pumping activity (Kutti et al, 2015) and consumption of organic matter (Leys et al, 2018), sponges play a major role in nutrient cycling (Maldonado et al, 2012), specifically in carbon turnover (Pile and Young, 2006;Yahel et al, 2007;Cathalot et al, 2015;Kahn et al, 2015), nitrogen flow (Hoffmann et al, 2009;Rooks et al, 2020) and the silicon cycle (Maldonado et al, 2020). Indeed, recently, studies point to serious impacts on ecosystem function when sponges are removed from the deep sea due to fishing bycatch (Pham et al, 2019).…”

Economic valuation of ecosystem services provided by deep-sea sponges

“…In situ benthic measurements of net sponge fluxes include a) sampling the water inhaled and exhaled by the sponges in either deep-sea habitats using manned submersibles and ROVs (Pile and Young, 2006) or in shallow water using scuba diving (Morganti et al, 2017), or b) sampling through incubation chambers that may target either sponge individuals that are isolated from the external environment (Maldonado et al 2020a, Maldonado et al, 2020bLópez-Acosta et al, 2019) or small portions of the bottom and its benthic community (Roth et al, 2019;Yates and Halley, 2003).…”