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Whale falls: chemosynthesis on the deep seafloor.

The deep seafloor is a biological desert--a region where animal biomass and production are typically supported only by the small rain of organic material arriving from productive surface waters thousands of meters above. In the late 1970s, however, deep-sea "oases" were discovered at hydrothermal vents. Here sulfide-rich effluents support dense communities of free-living bacteria, as well as tube worms and mollusks living in symbiosis with chemoautotrophic bacteria (internal bacteria that fix organic carbon using chemical energy from reduced compounds such as sulfide).

Similar communities were soon discovered at petroleum and sediment pore-water seeps, as well as in deep anoxic basins along oceanic margins (see Oceanus, Winter 1991/92). All these deep-sea "chemosynthetic" communities depend on geological "focusing" of reduced chemicals (such as sulfide or methane) at the seafloor, where bacteria can oxidize them to produce organic compounds that serve as food for higher organisms. Following these finds it seemed clear that such communities occur only along specific geological features, such as mid-ocean ridges and continental margins; the vast sediment plains of the abyss must indeed be deserts, devoid of even an occasional chemosynthetic oasis.

However, large concentrations of fresh organic matter can also yield substantial amounts of sulfide. In this case, anaerobic bacteria decompose the organic material, using sulfate (rather than oxygen) as an electron acceptor, and convert it to sulfide. This process produces dramatic odors at shallow-water sewer outfalls, and in theory could occur when large organic parcels, such as whale carcasses, sink to the nutrient-poor seafloor. Until recently, however, scientists had never observed organic-rich whale remains on the deep seabed.

This changed in 1987 when the research submersible Alvin chanced upon the lipid-rich skeleton of a 21-meter-long whale resting at 1,240 meters in the Santa Catalina Basin off the southern California coast. Subsequent visits to the skeleton in 1988 and 1991 revealed that the bones of this blue or fin whale were covered with thick bacterial mats similar to those observed at hydrothermal vents and seeps. The bone surfaces were also encrusted with a diverse assemblage of invertebrates, including mussels (Idasola washingtonia), limpets, snails, and polychaete worms. The sediments adjacent to the bones were sprinkled with dead shells from large vesicomyid clams, and numerous living clams (possibly Vesicomya gigas) peeped from sediments beneath bones. These clam, mussel, and limpet species are not normally found in the Santa Catalina Basin; nonetheless, they had achieved substantial population sizes (hundreds to thousands of individuals), and very large biomasses, on a single whale carcass.

Sulfide-Based Chemosynthesis

Several lines of evidence indicate that the whale-skeleton community in Catalina Basin is nourished, at least in part, by sulfide-based bacterial chemosynthesis. Studies conducted in the laboratory of microbiologist Jody Deming (University of Washington) revealed that the gill tissues of large vesicomyid clams and bone-encrusting mussels contain substantial amounts of enzymes that are characteristic of chemoautotrophic metabolism; transmission electron microscopy indicated that these enzymes were associated with endosymbiotic bacteria. After examining the carbon-13 and nitrogen-15 contents of the clam and mussel tissue, Steve Macko (University of Virginia) suggested that the clam derives all its nutrition from chemoautotrophy, while the mussel utilizes other energy sources as well (perhaps by feeding directly on whale-bone organics). Two other clam species collected at this whale skeleton (the vesicomyid Calyptogena pacifica and the lucinid Lucinoma annulata) are known to derive nutrition from endosymbiotic, sulfide-oxidizing bacteria. Thus, a substantial proportion of the rich, faunal assemblage at the whale skeleton seems to be supported by chemoautotrophic production.

What is the current sulfide source at the Catalina Basin skeleton, and why does the chemosynthetic assemblage hug the bones? The answers lie within the whale skeleton. To maintain buoyancy, the bones of living whales are rich in oils, as much as 60 percent lipid by weight. The central portions of the Catalina Basin bones still contain large lipid concentrations, which are being decomposed by anaerobic bacteria. The resulting reduced compounds (particularly hydrogen sulfide) diffuse outward through the bone matrix, providing an energy source for chemoautotrophic bacteria living on the bones and in the tissues of host animals such as clams and mussels.

Stepping Stones on the Seafloor?

An especially intriguing aspect of the Catalina whale-fall community is its taxonomic relationship to other chemosynthetic assemblages in the deep-sea. Components of this assemblage have been found on whale bones dredged from the deep sea off central and northern California, and, perhaps, from New Zealand (this, so far, is based are photographic evidence). In addition, two of the whale-fall limpets (Pyropelta corymba and Pyropelta musaica) and the mussel 1. washingtonia occur at hydrothermal vents; in fact, these limpets hail from the "fire limpet" family Pyropeltidae, originally thought to occur only at hydrothermal vents as grazers of sulfur bacteria. Some whale-fall species are also reported from wood falls in the North and South Pacific, and from anoxic sediments on the California slope. Thus, the whale-skeleton assemblage appears to be related to faunas from a broad range of chemosynthetic, deep-sea habitats, which are often geographically isolated and short-lived. One of the mysteries surrounding these communities concerns how this specialized fauna disperses between these ephemeral habitat "islands."

Calculations that suggest sulfide-rich whale falls may be surprisingly abundant (with an average spacing of about 25 kilometers in the deep north-east Pacific) lead to the hypothesis that whale falls might provide dispersal stepping stones for deep-sea dwelling species that are dependent on chemosynthesis. The large whale species, in combination, are cosmopolitan, so whale falls can occur virtually anywhere in the abyss. Sunken whale bones may thus provide oases for sulfide-dependent animals (especially hard-substrate species such as limpets) over vast reaches of open-ocean sediments. Discoveries last year of fossil chemosynthetic communities on fossil whale skeletons from the Olympic Peninsula suggest that whale falls may have provided dispersal stepping stones for more than 30 million years.

Important questions about deep-sea whale-fall communities remain unanswered, including: How rapidly do chemosynthetic communities develop when whale carcasses reach the seafloor, and how long do they persist? What proportion of the diverse species assemblages found at hydrothermal vents can actually colonize whale skeletons? We have initiated a research program to address these and related questions, using whale remains implanted in vent and nonvent deep-sea settings. The dead-whale material is obtained, with permission through the National Marine Fisheries Service, from cetaceans that die and become stranded on the California coast due to natural causes. We hope that these "burial-at-sea" experiments will soon help to shed light on the importance of whale carcasses as habitat islands for chemosynthetic communities at the deep seafloor.

Craig R. Smith is an Associate Professor in the Department of Oceanography at the University of Hawaii. He became interested in the oceans as a small boy living on a workboat in the Mediterranean Sea. His love for the sea was reinforced by years of schooling in the middle of Michigan. He now studies the ecology of the seafloor with his children Taina and Melanie on Hawaii's beaches, and with Alvin and surface ships in the deep ocean.
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Author:Smith, Craig R.
Date:Sep 22, 1992
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