An Empire Lacking Food
Once viewed as a barren expanse, the deep seafloor is a biologically elaborate ecosystem whose fate is tied to life above, near the sea surface
The Sum and Size of Deep-Sea Life
Edward Forbes is to deep-sea biology what Jean-Baptiste Lamarck is to evolution. Remembered for his mistaken stab at a theory of evolution, Lamarck concluded that an organism could alter a body part during its lifetime and pass this trait to offspring. Giraffes, in his view, stretched their necks to reach fruit high in trees, and the next generation inherited elongated necks. Despite his mistakes regarding how evolution works, Lamarck’s idea that change could be transmitted between generations was right.
Edward Forbes’s big mistake was concluding, in the mid-1800s, that marine life could not exist deeper than 550 meters, what he called the “azoic hypothesis.” Given the state of knowledge at the time, it seemed logical that no species could survive under the extremes of high pressure, lack of light, and cold temperatures characterizing the deepest ocean. Unsurprisingly, Forbes’s thinking spread quickly among the scientific community. The azoic hypothesis ultimately proved wrong, but much like Lamarck’s, Forbes’s ideas contained elements of truth. Forbes realized the importance of food to marine organisms; the lack of light and subsequent preclusion of plants in the deep led him to believe life could not exist there. He did not envision that material sinking from above could provide enough carbon for life to exist on the deep seafloor.
At the ocean’s surface, phytoplankton convert carbon dioxide into usable carbon through photosynthesis. Other organisms consume phytoplankton and in turn are consumed. This continuous feeding produces fecal material. And after enough time all organisms die. Feces, dead organisms and inorganic material shower the deep seafloor continuously. Polymers produced as waste by bacteria and phytoplankton hold these aggregates together. Combined, these form marine snow, the primary food source in the deep sea.
The arrival of marine snow to the seafloor is heterogeneous in both space and time. In coastal regions, phytoplankton production benefits from the upwelling of nutrient-rich waters toward the ocean’s surface. More production at the surface, generally, means more marine snow for the deep. In addition, as distance from shore and depth increase, marine snow must travel through more water to reach the seafloor, increasing the chances that organisms, from bacteria to bony fishes, will consume all or part of it.
In fairness, Forbes could not have been aware of marine snow; it was described well after his death. Nor was he aware of two other factors that form the backbone of modern theory on deep-sea ecosystems. First, biomass, the total weight of all life, on the seafloor closely correlates with the amount of carbon across the ocean’s surface and the subsequent amount of marine snow. In 2007, my colleagues and I reported that increases and decreases in biomass across the deep seafloor in the North Atlantic correlate tightly with variations in plankton production at the ocean’s surface. As a result, the highest biomass is found near coastal regions and in shallower depths—less than a few hundred meters. Through a stroke of unfortunate luck, Forbes sampled the deep eastern Mediterranean Ocean in an area now known to have extremely low primary production on its surface.
Second, dredges available for seafloor sampling in Forbes’s day were amazingly inefficient at capturing small organisms, which ultimately led him to miss a substantial share of the diverse deep-sea fauna. Just decades after Forbes’ pronouncement, Henry Nottidge Mosely wrote: “Some animals appear to be dwarfed by deep-sea conditions.” By the 1970s, Hjalmar Thiel of Universität Hamburg observed that the deep sea is a “small organism habitat.”
Depth is often viewed as a surrogate, albeit an imperfect one, for the variation in food across the deep seafloor because as previously mentioned, increased depth typically translates into less food. Thiel’s seminal 1975 work demonstrated that with increased depth, smaller organisms became more dominant. Deep-sea life falls into four faunal components based on size: megafauna, organisms such as fish, crabs, lobsters, starfish, urchins, sea cucumbers, sponges and corals, which are large enough to be photographed or caught in trawls; macrofauna, such as small polychaete worms, crustaceans and mollusks, which can be captured on a fine-mesh screen but are barely seen with the naked eye; meiofauna, such as forams, copepods and nematodes, which are retained only on very small mesh size; and, lastly, bacteria, the smallest of them all.
Thiel’s specific findings were that megafauna and macrofauna decrease more rapidly with depth than do meiofauna or bacteria. In fact, with increased depth meiofauna and bacteria become increasingly more dominant. Thus, at depths greater than 4 kilometers on the vast abyssal plains where food is extremely limited, there is a shift toward diminutive sizes. In a particularly striking example of this, my doctoral advisor Michael Rex of the University of Massachusetts at Boston and I calculated that our entire collection of deep-sea gastropods from the western North Atlantic— over 20,000 shells—could fit completely inside a single Busycon carica, a fist-sized New England knobbed whelk.
But to say that all creatures of the deep are miniaturized overlooks the complexity of size evolution in this unique habitat. One of the puzzles I faced early in my research was that despite overall miniaturization of deep-sea invertebrates, some taxa actually obtain much larger sizes, approaching gigantism. For example, although deep-sea snails are smaller than their shallow-water relatives, they actually increase in size with greater depth and presumed lower food availability. To further confound the situation, other scientists have reported the exact opposite pattern in other types of snails, whose size decreases with depth. The same appeared to be true in other taxa, such as crustaceans. A question emerged: What biological processes produced these fundamentally opposing trends in body-size evolution?
To answer that, I turned from the Earth’s largest habitat to one of its smallest —islands. Body-size extremes are well documented on islands. The diminished kiwi and the enormous moa of New Zealand, the colossal Komodo dragon on the island of Komodo, the extinct pygmy elephants on the islands of the Mediterranean, the ant-sized frog of the Seychelles, the giant hissing cockroach of Madagascar and the giant tortoise of the Galapagos represent just a few of the multitudes of island size anomalies. In 1964, J. Bristol Foster of the University of East Africa demonstrated that large mammals became miniaturized over time on islands. Conversely, small mammals tended toward gigantism. This occurs with such frequency that scientists refer to it as “Foster’s rule” or the “island rule.” Fewer predators, less competition from other species, reduced habitat area and potentially marginal food sources are all hypothesized to produce these new and sometimes bizarre evolutionary trajectories.
My colleagues and I discovered a similar pattern in 2006 between shallow and deep seas. As shallow-water gastropods evolved into deep-sea dwellers, small species became larger and large species became smaller. Interestingly, size did not shift in a parallel manner. Larger taxa became disproportionately smaller sized—that is, both converged on a size somewhat smaller than medium. I’ve since observed this pattern in radically different taxa, such as bivalves and sharks.
The fact that islands and the deep sea have so little in common suggests that the explanation rests with a single trait both habitats share. A paucity of total food likely drives complicated body-size trajectories in the deep sea as well as on islands. On islands, less food is available because smaller land areas support fewer plants at the base of the food chain. In both habitats, there may not be enough total carbon to support populations of giants only. Unable to travel long distances to search for food or to store large fat reserves to fast through periods of food scarcity, smaller organisms are also at a disadvantage. If these contrasting selection pressures were equal, size would be driven to an intermediate. However, the selection against larger sizes is greater, leading toward an evolutionary convergence that is slightly smaller than the intermediate size. Thus, differential responses to food reduction by different-sized organisms may resolve the outstanding paradox of divergent size patterns in the deep.
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