Relationship between geochemical environments, nutritional resources, and faunal succession in whale-fall ecosystems

Abstract

Faunal succession in whale-fall communities is closely associated with the progress of decomposition of the whale carcass. The main nutritional resources supporting a whale-fall community change from whale matter to chemosynthetic products over time. To study the geochemical aspects of this nutritional succession, we sampled animals over time on and in sediments around carcasses of sperm whale Physeter macrocephalus in Sagami Bay (mobile scavenger to early sulfophilic stage) and off Cape Nomamisaki (sulfophilic stage), Japan (500 and 200-300 m water depths, respectively). In these 2 areas, stable carbon, nitrogen, and sulfur isotopes of the animal soft tissues were measured to precisely elucidate the nutritional resources for each animal. In Sagami Bay, mobile scavengers relied only on whale soft tissue. Infaunal animals at 2 wk after the deployment relied only on whale soft tissue, while infauna at 9 mo after the deployment relied on chemosynthetic products. Such changes in nutritional resources were consistent with the transition of the geochemical environment in the sediments. Off Cape Nomamisaki, vigorous microbial sulfate reduction and thioautotrophic primary production nourished the fauna around the carcasses. The fauna in this area consisted of chemosymbiotic bivalves and necrophagous animals with sulfide-tolerant metabolism. We conclude that the changes in microbial processes, biomass, and compositions in sediments influence faunal succession in whale-fall ecosystems via change in the available nutrition for the fauna.

Cryptic fungal diversity revealed in deep-sea sediments associated with whale-fall chemosynthetic ecosystems

“…Whale-falls produces unique organic and sulphide-rich habitat islands at the seafloor. Giant body sizes and especially high bone-lipid content allow great whale carcases to support a sequence of heterotrophic and chemosynthetic microbial assemblages in the energy-poor deep sea (Smith et al 2015 ; Onishi et al 2020 ). Since the first recognition of the whale-fall chemosynthetic ecosystems in deep sea off California by Smith et al ( 1989 ), it is known that metazoan communities in whale-fall ecosystems contain many new species and evolutionary novelties, including bone-eating worms and snails with faunal overlap with other deep-sea chemosynthetic communities, such as hydrothermal vents, cold seeps and wood falls (Fujiwara et al 2010 ; Sumida et al 2016 ).…”

Major contribution of sulfide‐derived sulfur to the benthic food web in a large freshwater lake

“…Carbon and nitrogen isotopic ratios (δ 13 C and δ 15 N) are useful for ascertaining the trophic position of taxa and the trophic structure of communities (DeNiro & Epstein, 1981;Minagawa & Wada, 1984). However, S isotopic compositions (δ 34 S) are used to trace diet resources, especially primary S resources, because of the slight isotopic fractionation during assimilation, similar to that of carbon (Onishi et al, 2020;.…”

“…Hydrogen sulfide in sediment and the amorphous iron sulfides formed by this reaction are collectively designated as acid volatile sulfide (AVS) (Berner, 1964; Rickard & Morse, 2005). The SOB biomass fueled by AVS is an important diet resource for benthic animals in some environments, such as cold seeps and hydrothermal vents (Onishi et al, 2020; Onishi, Yamanaka, et al, 2018; Yamanaka et al, 2015). Despite the occurrence of sulfide by MSR and putrefaction even in freshwater environments with low‐sulfate concentrations (typically 0–2.5 mmol L −1 , mostly <1 mmol L −1 ; Fry, 1986; Jones et al, 1982; Zak et al, 2021), effect of the SOB on benthic food webs remains unclear because of inadequate interest and research methods.…”

“…Carbon and nitrogen isotopic ratios ( δ 13 C and δ 15 N) are useful for ascertaining the trophic position of taxa and the trophic structure of communities (DeNiro & Epstein, 1981; Minagawa & Wada, 1984). However, S isotopic compositions ( δ 34 S) are used to trace diet resources, especially primary S resources, because of the slight isotopic fractionation during assimilation, similar to that of carbon (Onishi et al, 2020; Onishi, Yamanaka, et al, 2018). The three potential food resources of sinking particles (i.e., photoautotrophic product), MOB, and SOB in benthic food webs can potentially be distinguished isotopically.…”