Seven-year enrichment: macrofaunal succession in deep-sea sediments around a 30 tonne whale fall in the Northeast Pacific

Abstract

Whale falls cause massive organic and sulfide enrichment of underlying sediments, yielding energy-rich conditions in oligotrophic deep-sea ecosystems. While the fauna colonizing whale skeletons has received substantial study, sediment macrofaunal community response to the geochemical impacts of deep-sea whale falls remains poorly evaluated. We present a 7 yr case study of geochemical impacts, macrofaunal community succession, and chemoautotrophic community persistence in sediments around a 30 t gray-whale carcass implanted at 1675 m in the well-oxygenated Santa Cruz Basin on the California margin. The whale fall yielded intense, patchy organic-carbon enrichment (>15% organic carbon) and pore-water sulfide enhancement (> 5 mM) in nearby sediments for 6 to 7 yr, supporting a dense assemblage of enrichment opportunists and chemosymbiotic vesicomyid clams. Faunal succession in the whale-fall sediments resembled the scavenger-opportunist-sulfophile sequence previously described for epifaunal communities on sunken whale skeletons. The intense response of enrichment opportunists functionally resembles responses to organic loading in shallow-water ecosystems, such as at sewer outfalls and fish farms. Of 100 macrofaunal species in the whale-fall sediments, 10 abundant species were unique to whale falls; 6 species were shared with cold seeps, 5 with hydrothermal vents, and 12 with nearby kelp and wood falls. Thus, whale-fall sediments may provide dispersal stepping stones for some generalized reducing-habitat species but also support distinct macrofaunal assemblages and contribute significantly to beta diversity in deep-sea ecosystems.

Diversity, Distribution and Phylogeny of Hesionidae (Annelida) Colonizing Whale Falls: New Species of Sirsoe and Connections Between Ocean Basins

“…Whale carcasses impact the food-limited deep sea (>200 m) creating remarkable island-like habitats considered hotspots of biodiversity and evolutionary novelty (Smith and Baco, 2003;Smith et al, 2015). Assemblages of opportunist and specialist fauna colonize carcasses during overlapping successional stages and also on the mosaic of microhabitats formed on the skeleton and surrounding sediments (Baco and Smith, 2003;Smith and Baco, 2003;Fujiwara et al, 2007;Lundsten et al, 2010b;Smith et al, 2014Smith et al, , 2015Alfaro-Lucas et al, 2017). Whale falls have been hypothesized to act as ecological and evolutionary stepping stones for some chemosymbiotic hydrothermal vent and cold seep fauna, such as vesicomyid and bathymodiolin bivalves (Smith et al, 1989(Smith et al, , 2015(Smith et al, , 2017Distel et al, 2000;Smith and Baco, 2003;Lorion et al, 2009Lorion et al, , 2013Miyazaki et al, 2010;Kiel, 2017).…”

Comparative study of vent and seep macrofaunal communities in the Guaymas Basin

“…Although seeps and vents belong to two different geological contexts, both ecosystems are characterised by fluid emissions that present unusual properties, such as the presence of high concentrations of toxic compounds, steep physicochemical gradients and significant temporal variation at small spatial scales (Tunnicliffe et al, 2003). Furthermore, they both generate energy-rich fluids that sustain high local microbial chemosynthetic production in deep-sea ecosystems, which are usually food-limited (Smith et al, 2008). There, bacteria and archaea rely mainly on the oxidation of methane and hydrogen sulfide, which are the two most common reduced compounds in vents and seeps (McCollom and Shock, 1997;Dubilier et al, 2008;Fisher, 1990).…”

Comparative study of vent and seep macrofaunal communities in the Guaymas Basin

“…Growing evidence of evolutionary and functional homologies rapidly highlighted potential links between the two ecosystems. Further support for this hypothesis was provided by the presence of species shared between seeps and vents and by the discovery of additional chemosynthetic stepping-stones such as large organic falls (Smith and Baco, 2003;Smith and Kukert, 1989). Moreover, macrofaunal communities at a recently discovered hybrid seep and vent ecosystem called a "hydrothermal seep", associated with a subducting seamount on the convergent Costa Rica margin, harbours both seep and vent features, thus providing additional support for the hypothesis of continuity among reducing ecosystems .…”

“…Although seeps and vents belong to two different geological contexts, both ecosystems are characterised by fluid emissions that present unusual properties, such as the presence of high concentrations of toxic compounds, steep physicochemical gradients and significant temporal variation at small spatial scales (Tunnicliffe et al, 2003). Furthermore, they both generate energy-rich fluids that sustain high local microbial chemosynthetic production in deep-sea ecosystems, which are usually food-limited (Smith et al, 2008). There, bacteria and archaea rely mainly on the oxidation of methane and hydrogen sulfide, which are the two most common reduced compounds in vents and seeps (McCollom and Shock, 1997;Dubilier et al, 2008;Fisher, 1990).…”