This story begins where a whale’s life ends.

In life, the whale reigns supreme and powerful—our connection to a lost world of dinosaurs and the sea, a symbol of what is great, free, and intelligent. In death, the whale continues an act of stately splendor. It produces a funereal procession that’s been enacted for millions of years, but one for which we are just getting snapshots of now. Credit for what we do know about the remarkable afterlife of the whale is largely due to the efforts of biological oceanographer Craig Smith of the University of Hawaii and his research associates, including graduate student Amy Baco.

For more than a decade, Smith has been pursuing the idea that whale corpses (called whale falls when they fall to the bottom of the ocean) serve as biological stepping stones for a host of exotic deep-sea animals that survive in some of the world’s harshest environments. His theory has stirred debate among scientists trying to determine how tube worms, clams and other colonizers of hydrothermal vents and cold seeps arrive and persist in their ephemeral habitats. Smith believes that for the past 30 million years or so, whale falls may have been providing a stepping stone for at least some of these animals to colonize over vast expanses of the ocean.

Studying whale falls has important implications for science. “If we want to understand how evolution works, we need to explain the incredible diversity of animals in the deep sea,” said Smith. At least 16 animal species new to science have been found in the 13 years that Smith and other scientists have been studying whale falls. Biodiversity also means there are lots of genetic resources with potential commercial applications to tap. For example, a San Diego biotechnology company is working with Smith to develop a cold-water detergent containing an enzyme found in bacteria growing on whale bones. Such a detergent may have the potential to yield substantial energy savings on a national scale. Understanding what happens to organic-rich matter in the deep sea--like a 35 ton whale--is another area of broad ecological interest. This knowledge is relevant both for understanding how deep sea animals respond to point-source enrichment and for predicting the effects of relocating sewage sludge or disposing of other organic-rich wastes at the deep-sea floor, Smith said.

Skeleton of a 35-ton, 13-m gray whale that has been at the Santa Cruz Basin seafloor (~1700 m deep) for 18 months. This carcass is at the transition between the mobile- scavenger and enrichment-opportunist stages. Animals visible include swimming, eel-like hagfish, and thousands of amphipods and newly settled, juvenile clams (both white specks on the sediment).

Both Buddhists and Hindus share the idea of reincarnation, which in its simplest form means that life does not end with death. In the whale’s case, life is attracted and then emerges from the whale’s corpse creating a lush faunal island in the ocean abyss. It was by chance, in 1987, that Smith and co-workers first stumbled upon whale a skeleton at the bottom of the Santa Catalina Basin in the submersible Alvin. What impressed the oceanographers were the bacterial mats and clam shells around the whale bones—clams similar or identical to some that occur at hydrothermal vents.  The sulfide-rich waters of these vents, which occur at the world’s mid-ocean ridges, are inhospitable to most animals. Only a  decade had passed since the discovery of the vents, vent fauna and their astonishing biology. These animals harbor bacteria that are capable of using energy from toxic hydrogen sulfide in vent fluids to produce organic matter the animals can consume in a process known as chemoautotrophy. In subsequent expeditions, researchers found chemoautotrophic communities at ocean floor hot springs along the spreading centers of the world’s plates. Similar communities fueled by sulfide or methane were found at sites of oil, brine or pore-water seepage associated with petroleum-rich sediments, subduction zones, submarine canyons, carbonate scarps and turbidites in the Atlantic and Pacific Basins, Smith said.

Now Smith was observing animals similar to those found at hydrothermal vents and cold seeps on a whale skeleton, and he wondered what chemical substances in its bones were supporting life. Working in the Santa Catalina Basin off the coast of Los Angeles, Smith’s research team studied a whale skeleton 1240 meters beneath the sea. What the researchers learned was that whale bones, up to 60 percent lipids (fats) by weight, provide a hefty meal for a host of organisms. Bacteria decompose the fat anaerobically, emitting hydrogen sulfide. Thick mats of chemoautotrophic bacteria live off the sulfide, in turn supporting worms, mollusks, crustaceans, and other animals.  Twelve years later these communities are still going strong, Smith said.

Hagfish swimming over ALVIN's instrument basket at the floor of the Santa Cruz Basin. The skeleton of a gray whale whale is visible in the background. The instruments in the basket are used for collecting samples of seafloor sediments and associated animals.

The discovery of whale falls and fauna sent Smith off on a path that continues to captivate the attention of scientists, and gradually, a greater audience. This February, the journal Nature will publish the latest paper on the subject of whale falls. Thirteen years have passed since Smith and collaborators first proposed in Nature that whale bones may provide a stepping stone for the introduction of species to vents. Now there is strong evidence.

DNA analysis enabled Smith and his coauthors to demonstrate a close genetic relationship between mussels, including Idas washingtonia, found on deep-sea wood and whale bones and those from hydrothermal vents. Like whale falls, wood falls produce intense pockets of organic enrichment at the seafloor, attracting chemoautotrophic species, Smith said. In fact, the mussels they found at wood and whale fall sites share the same subfamily (the Bathymodilinae) with mussels from vents and seeps, and one species from whale/wood falls appears to be the most primitive member of this group. This  suggests that mussels may have used whale falls and/or wood falls as evolutionary stepping stones between shallow-water habitats (such as salt marshes) and hydrothermal vents in the deep sea.  Coauthors on the paper are Daniel Distel of the University of Maine, Amy Baco of the University of Hawaii, and Wendy Morrill and Colleen Cavanaugh of Harvard University. The research was supported, in part, by the NOAA'sl Undersea Research Program (NURP).
 

Understanding the phases of colonization by animals at whale falls is another focus of Smith’s research supported by NURP. In June 1998, Smith and his colleagues used the research submersible Alvin to study one natural and three experimentally implanted whale carcasses off the coast of southern California. They would examine a 10,000 kg. gray whale implanted at 1,900 m in the San Clemente Basin in 1992, a 5,000 kg. gray whale implanted at 1,220 m in the San Diego Trough in 1996, and 35,000 kg. gray whale emplaced at 1,750 m in the Santa Cruz Basin in May 1998. They would observe the whale falls during submersible visits to the carcasses at time intervals between 10 and 120 days as well as between one, three, five and 10 years.

Whale falls pass through three successional stages, the researchers discovered. The first stage is dominated by mobile scavengers. “There are dense aggregations of hagfish, small numbers of lithodid crabs (a new species of crab found at whale falls), rattail fish, large sleeper sharks, and millions of amphipods,” Smith said. “This stage can be surprisingly short with more than 90 percent of the soft tissue stripped from the 5-ton carcass within four months.” On larger whale carcasses, like the 35,000 kg. Santa Cruz whale, this stage lasts at least nine months and could persist for more than two years, he said.

The next phase whale falls enter is called the enrichment-opportunist stage. During this period whale skeletons are surrounded to several meters by dense aggregations of polychaete worms and cumaceans. Densities of these species are the highest ever measured in the deep-sea below 1,000 m.  At least two of the extremely abundant species near the whale skeleton are new to science and may be whale-fall specialists, according to Leslie Harris, collection manager of the Los Angeles County Museum of Natural History.

This polychaete worm, discovered by Smith at a whale fall in the Santa Cruz basin, is new to science and may be a whale fall specialist.

Last October, Smith and Baco used an ROV to return to the whale fall study sites. Smith brought samples of the worms found at the whale implants in the Santa Cruz basin to Harris for identification. "These are big, beautiful, and bizarre worms,” said Harris, referring to the 50 mm long worms, which resemble centipedes, found in the Santa Cruz basin. The museum where she works holds the largest collection of polychaetes in the world. At first she couldn’t find another worm like it until she turned to an obscure paper by a Russian researcher characterizing a polychaete that lived in the anoxic Black Sea. Conditions at a whale skeleton may be comparable, Harris said. “This worm exhibits wonderful behavior that nobody knows about,” she said, noting that in video footage she received from Smith she observed the worms hanging on the whale carcass in such dense aggregations that they looked like a shag carpet.  Finding out about this new polychaete will be an important step for science.  The worms appear to play a major role in structuring the newly discovered deep-sea community found at whale falls. How these worms arrive at whale falls and what role they play in the food chain there are totally unknown. Since polychaete worms have existed for millions of years and have an incredible diversity of lifestyles, they’re an important group for learning more about evolution, Harris said.

After the worms disappear from the whale carcass, the whale fall enters its last stage. This stage is also the longest—continuing in excess of ten years. It is called the sulfophilic stage because of the abundance of species thriving off the sulfide produced by whale bones. The decay of bone lipids supports remarkably dense bacterial mats, mussels, vesicomyid clams and occasionally vestimentiferan tube worms. During this stage researchers found more than 30,000 animals in a broad range of taxa on a single skeleton, Smith and Baco said. The diversity of species found in these dense populations far outnumber local species richness in other extreme deep-sea environments including hydrothermal vents, cold seeps, and manganese nodules. In fact, the population at the whale falls rivals the species-rich rocky intertidal habitat.

A whale bone being recovered from the Santa Catalina Basin floor five years after experimental emplacement. The bone surface contains patches of white bacterial mats and a squat lobster (or galatheid crab). Hydroids have sprouted on the loop of yellow line attached to the bone.

Genetic studies at the whale fall sites indicate that the animals at whale skeletons are closely related to the animals found at hydrothermal vents and cold seeps. “DNA studies of the

Idas washingtonia from deep sea whale bones and wood falls reveal a surprisingly close  relationship to the Bathymodiolinae, the subfamily of mussels previously considered to be restricted to hydrothermal vents and cold seeps,” according to Smith and his research team. 

Ancestors of the mussels may have moved into the deep sea along with organically-rich wood and whale falls, and then made “the relatively small ecological leap from these sites to sulfide rich vents and cold seeps at the deep sea floor,” Smith said. “In total, California whale falls are now known to share 10 species with vents, nine with seeps, four with anoxic sediments and one with wood falls,” Smith said. “Thus, the ecology and evolution of whale skeletons communities clearly are related to those of other deep sea reducing habitats.”

A whale is cosmopolitan during its life traveling freely around the globe. Its death in a random part of the deep sea  is punctuated by remarkable energy. Little understood animals appear to materialize from nowhere upon the whale’s arrival.
Despite the enormous logistic difficulties of towing and sinking decomposing whale caracasses, Smith’s research offers a glimpse into this mysterious process. He did succeed in getting the support needed to sink a 35,000 kg. gray whale carcass.  This site will be used to study whale fall succession on the “truly leviathan scale” for years to come, Smith hopes.

Smith would like to continue monitoring the whale falls in intervals of two, three and 17 years. The researcher has implanted kelp and wood falls near the whale falls. Since the San Clemente seep is only 50 to 120 km up current from the site of the whale, wood and kelp falls, the seep fauna may be a likely source of colonists for these sites. The genetic relationship between whale falls, cold seeps, kelp falls and wood falls, as well as how long these communities persist, remains poorly known. Smith’s research will help elucidate the role whale falls play in deep-sea processes. “These processes have fueled speculation for decades, but can now be studied," he said.
 

Additional information about this project can be found by contacting Craig Smith at the University of Hawaii Department of Oceanography, 1000 Pope Road, Honolulu, HI 96822 or by email to csmith@soest.hawaii.edu. The Research was supported through a grant from the NOAA's Undersea Research Program's West Coast and Polar Regions Undersea Research Center. Additional funding was provided by the National Science Foundation.