Deep-Ocean Life Where Oxygen Is Scarce

Home , Gnathophausia ingens, Oxygen minimum zone

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Oxygen-deprived zones are common and might become more so with climate change. Here life hangs on, with some unusual adaptations

Lisa A. Levin

n 1925, the Meteor expedition set out cano 7, a submerged mountain about region of the ocean containing less than Ifrom Germany to measure the ocean’s 200 miles west of Acapulco, Mexico. 0.5 milliliter of oxygen per liter of wa- depth, study marine chemistry and, on The seamount has its summit 730 meter. It is surprising that any life exists the side, extract gold from seawater. The ters below the surface and its base where the oxygen supply is so sparse. gold project didn’t pan out, but expedi- 3,400 meters deep. With a group of ge- In addition to the OMZs that lie off tion data revealed a curious feature in ologists, I first visited Volcano 7 in 1984 the western coasts of the Americas, the Atlantic, off southern Africa: a giant to photograph and study the moun- well-established OMZs have also been wedge of oxygen-deficient water 300 to tain’s slopes using Alvin, a submersible discovered in the Arabian Sea, the Bay 400 meters down. vehicle based at Woods Hole Oceano- of Bengal and off the western coast of The surface layers of the ocean gener- graphic Institution (WHOI), and AN- Africa. In the United States, the zones ally obtain oxygen from diffusion and GUS, a camera mounted on a sled. I lie off California and Oregon. Califor- brisk circulation. This water sinks to the noticed the fascinating sea life, but we nia’s Santa Barbara Basin, with its bot- seafloor, supplying oxygen to deep-sea did not measure oxygen on that trip. tom at 585 meters, is right within the life. But sluggish circulation and oxy- Four years later, I returned with a California OMZ and has very little gen-poor source waters can reduce oxy- group of women who were studying oxygen. My group at North Carolina gen concentrations at intermediate plankton and life on the ocean floor. State University and then at Scripps In- depths. In several oceans, this effect is Again, we employed Alvin to explore stitution of Oceanography, in collabo- unusually pronounced. Where primary the volcano’s surface. ration with U.S. and international in- production by photosynthetic life is Because Alvin had space for only a vestigators, has studied OMZs off very high, the decay of sinking organic pilot, two scientists and our gear, we California, Mexico, Peru, Chile and matter consumes so much oxygen that had to squeeze down on our knees and Oman. Using data on seafloor topog- the middle depths contain dramatically peer sideways to look through a port- raphy and oxygen measurements from less of the gas than water above or be- hole. The vehicle’s exterior lights, the National Oceanographic Data Cen- low. Such oxygen-minimum zones, or though powerful, illuminated only six ter, we recently teamed up with John OMZs, turn up in productive open to eight feet of water, focusing our Helly at the San Diego Supercomputer oceans and on continental margins. attention on the fauna at hand rather Center to estimate how much of the They can stretch for thousands of miles than the larger view. At about 800 me- continental margin seafloor is inter- and persist for thousands of years. ters below the surface, dense group- cepted by OMZs. Our global estimate I first encountered an OMZ while ings of crabs, shrimp, brittle stars and was about 2 percent. studying animal communities on Vol- sponges were zoned like invertebrates Seasonal oxygen-depleted zones are on a rocky shoreline. But as we moved also known. Water over the shallow Lisa A. Levin is a biological oceanographer in the up the mountain’s slope, the rocks sud- shelf off Chile becomes depleted dur- Integrative Oceanography Division at Scripps In- denly looked barren, covered with the ing the spring and summer, when it is stitution of Oceanography. She completed her Ph.D. merest fuzz of life fed by the poorly oxygenated Peru- at SIO in 1982 and then, after a year of postdoctoral Wondering what might account for Chile Undercurrent. In fall and winter, study at Woods Hole Oceanographic Institution, the dramatic change, we looked at the it becomes oxygenated again as cold, accepted a faculty position at North Carolina State oxygen data generated by a sensor sub-Antarctic currents prevail. Human University. In 1992, with their children, she and mounted on the submersible’s shell. A activities deplete other bodies of water. her oceanographer husband returned to SIO, where liter of seawater can hold 7 or more In some estuaries and coastal regions, both are now professors. She studies the ecology of milliliters of oxygen. (For comparison, fertilizer runoff or sewage outfall pro- animal communities in marine sediments, particu- a liter of air can hold 210 milliliters of motes periodic phytoplankton blooms, larly those of stressed environments, from the inter- tidal zone to the deep sea. Address: Integrative oxygen.) But the water that swathes which rob the water of oxygen as they Oceanography Division, Scripps Institution of the peak of Volcano 7 contains less decay. Such human-inspired hypoxic Oceanography, 9500 Gilman Drive, La Jolla, CA than one-seventieth of that amount— events have taken place in many parts 92093-0218. Internet: [email protected]; 0.1 milliliter per liter. The seamount of the world, including Chesapeake http://levin.ucsd.edu summit protrudes into a vast OMZ—a Bay, the New York Bight and the Gulf

foraminifera sponges galatheid crabs

serpulid worms

upper summit shrimp

brittle stars

rattail lower summit

pillow lava

sponges

flank

xenophyophores

bottom

Figure 1. Oxygen-minimum zones, such as the one atop Volcano 7 in the eastern Pacific west of Acapulco, Mexico, are permanent features of several oceans. They are found at intermediate depths and can stretch for thousands of miles. With an oxygen content one-fourteenth or less that at the surface, they provide habitats where certain marine organisms can enjoy abundant food and freedom from predators. Single-celled creatures in the order Foraminifera and minute worms called nematodes dominate the summit of Volcano 7. Farther down the seamount, near the lower boundary of the oxygen-minimum zone, the still-plentiful food supply and slightly higher oxygen concentrations support larger organisms such as seapens, sponges and shrimp. The density of animals at this lower boundary can be several times higher than the density farther down the volcano.

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 2002 September–October 437 with permission only. Contact [email protected]. of Mexico. A severe hypoxic event in the northern Adriatic in 1977 slaugh- tered masses of marine organisms. Understanding the formation and ecological impact of oxygen-depleted zones is critical because their number and intensity are likely to increase as global warming and nutrient enrich- ment rob the ocean of oxygen. Because such zones are inhospitable to animals we consider edible, their expansion could have a devastating effect on commercial fishing.

OMZs: What, Where and Why OMZs generally form where winds cre- ate currents that move water along a continent’s western shoreline. Aided by the Earth’s rotation, such currents Figure 2. Extensive oxygen-minimum zones (gray) have arisen off the west coasts of North, sweep water offshore. Replacing the Central and South America, off southwest Africa, and in the Arabian Sea and Bay of Bengal. It lost mass, cold water rises up from the has been estimated that about 2 percent of the continental margin seafloor lies below such ocean’s depths. It brings nutrients, es- zones, which consist of midlevel waters depleted of oxygen by the decay of organic matter pecially nitrogen, to the sunlit surface, from highly productive surface waters. Incoming currents do not replenish them because they where a lack of nutrients would other- are also oxygen-poor. The map also includes hypoxic zones, such as those in the Black and wise limit plankton and nekton growth. Baltic seas, that have arisen by different processes. When the resulting glut of surface- 0 dwelling organisms dies, the bacterial garbage recyclers of the ocean deplete the water of oxygen as they degrade the detritus. If such conditions persist 50 for long periods, middle depths can become permanently short of oxygen, < 0.01–0.1 and an OMZ can appear. Areas that lack a constant supply of 1,00 oxygenated water are good candidates 0.1–0.5 for OMZ formation. For example, the eastern Pacific and Indian oceans re- ceive water from the North Atlantic, 0.5–1.0 1,50 where most new deep water forms. As this water travels south for hundreds of years, it loses oxygen. The Arabian 2.0 Sea, which contains a vast OMZ, also receives poorly oxygenated waters,

depth (meters) 2,00 which come from the Red Sea, Persian Gulf and Banda Sea. Interested in the adaptations of sea- 2,500 floor communities to extreme environments, I began to study OMZs in 1988, 3.0 when groups led by Karen Wishner (University of Rhode Island), Marcia Gowing (University of California, Santa 3,000 Cruz), Lauren Mullineaux (WHOI) and myself visited the slopes of Volcano 7 aboard WHOI’s research vessel Atlantis II. Because OMZs usually lie between 200 and 1,300 meters, they can inter- 10020 10 30 cept the seafloor on seamounts and distance from seamount summit (kilometers) edges of continents. Figure 3. Oxygen concentrations rise with depth along the slope of Volcano 7. The volcano’s Descending through an ocean con- summit protrudes into an oxygen-minimum zone, where oxygen concentrations range from taining an OMZ, you encounter a wide near zero to 0.5 milliliter of oxygen per liter of seawater (darker blues). At the volcano’s base, range of oxygen concentrations. The the oxygen concentration is much higher, at 3 milliliters per liter. This zonation shapes the first part of your journey takes you communities of animals on Volcano 7 (Figure 1). down through well-oxygenated water,

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 438 American Scientist, Volume 90 with permission only. Contact [email protected]. which persists for 500 to 1,000 meters off the coast of Central America or Peru and for up to 400 meters off the coast of Oregon or California. In waters off Mexico, the first 100 meters is sunlit, so you see small planktonic organisms. Once you enter the OMZ, the oxygen content drops precipitously to below 1 milliliter of oxygen per liter of water, placing you in a low-oxygen— dysoxic—zone. At 300 to 700 meters, the water’s oxygen content stabilizes at its lowest level, forming a microxic (less than 0.1 milliliter per liter) zone. Oxy- gen gradually becomes more plentiful again as you continue to descend. But if you reach the seafloor while still within the zone, you find soupy mud off Oman, sand made of shells on the slopes of Volcano 7, and fine sediment with phosphorite rocks off Peru. These sediments are rich in nutritious debris. Figure 4. Scientists sample the ocean floor by lowering corers into marine sediments. To separate organisms of different sizes, they sieve sediments through progressively finer meshes. Adapting to Oxygen Deprivation These polychaete worms were retained by a 300-micron sieve and therefore are part of the The abundance of nutrients, combined macrofauna. They were retrieved from a depth of 448 meters in the oxygen-minimum zone off with diminished competition for food the coast of Oman, where the oxygen concentration was 0.13 milliliter per liter. The worms are and fewer predators, offsets some of transparent, but the ones in this photograph were stained with a pink dye called rose bengal. the disadvantages of OMZs for organ- The dominant polychaete at this depth is a worm in the genus Prionospio (see Figure 6). (Pho- isms that can adapt to this unusual mi- tograph courtesy of Peter Lamont, Scottish Association for Marine Science.) lieu. As might be expected, these adaptations can also be highly unusual. For drogen sulfide. Because zones of sul- mud and facilitate water movement by example, giant bacteria that use nitrate fide and nitrate do not overlap, the bac- constructing nests, mudballs or tubes. to oxidize hydrogen sulfide are con- teria commute up into seawater to ob- Nancy K. Sanders and James Chil- spicuous in OMZs. Their chemical ex- tain nitrate. Swaying back and forth dress of the University of California, pertise enables them to obtain energy and emerging from their sheaths, they Santa Barbara, studied the adaptive without the need for oxygen. The re- form a quivering, white lawn. features of Gnathophausia ingens, a sulting crystals of elemental sulfur ac- Heide Schulz, with an international large red mysid that squirts lumines- cumulate, making the cells look white. team of scientists aboard the Russian cent material when disturbed. This Two sulfur-oxidizing bacteria, Thioploca research vessel Petr Kottsov, recently shrimp is common in OMZs. Impor- and Beggiatoa, are common in sedi- discovered an even larger sulfur-oxi- tant features include excellent ventila- ments under OMZs off northern Chile, dizing bacterium in sediments off tion, a large surface area on the gills, Peru, Oman, Namibia and Pakistan. Namibia. Thiomargarita namibiensis has minimal separation between seawater Thioploca cells align in long filaments pearly spheres for cells that can reach and the blood flowing through the that look like angel-hair pasta. The fila- three-fourths of a millimeter—almost gills, the ability to remove up to 90 ments glide through the water in slimy twice the size of the period at the end percent of oxygen from inhaled water, sheaths and, in some locations, form of this sentence. These cells also grow brisk interior circulation and an effi- dense, yellow mats. in chains, but they are not motile. T. cient respiratory pigment. Thioploca was first found by Chilean namibiensis holds the world record for Unusually adept respiratory pig- scientist Victor Gallardo in the OMZ bacterial size, being about 3 million ments appear to be an adaptation to under the Peru-Chile Subsurface Coun- times larger than most bacteria. OMZs. The blue pigment hemocyanin tercurrent system, where it colonizes Rather than circumventing the need has more extreme properties in G. in- more than 10,000 square kilometers of for oxygen, other organisms have gens from the OMZ off California continental shelf. Like Beggiatoa, its cells adapted to OMZs by developing high- than in G. ingens from Hawaii, where form filaments. But dozens of fila- ly efficient ways to extract oxygen from oxygen concentrations are higher. Its ments—and even filaments of different depleted water. Bottom-crawling crus- very high affinity for oxygen enables Thioploca species—share a sheath. Off taceans in the genus Ampelisca have it to snatch the gas from oxygen-poor the Chilean coast, Thioploca constructs gills with a large surface area, as do water, but other properties allow it to thick, gelatinous mats on the seafloor OMZ-dwelling mysids (small shrimp- release oxygen readily to tissues. An that can weigh up to 120 grams—about like animals), fishes and cephalopods. unusual insensitivity to changing a quarter of a pound—per square me- Polychaete worms have extensive long temperature keeps the pigment func- ter. Vertical mucous tunnels under the tentacle-like branchiae that presum- tional at different depths. The respira- mats allow Thioploca filaments to slide ably facilitate oxygen uptake. Inverte- tory pigment hemoglobin, which col- down into the sediment and find hy- brates in OMZs often stabilize sloppy ors vertebrates’ red blood cells, is

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 2002 September–October 439 with permission only. Contact [email protected]. Figure 5. Members of the order Foraminifera that can tolerate low oxygen conditions are important inhabitants of oxygen-minimum zones, where their abundance relates to the availability of organic debris. They are among the few classes of organisms with shells that have adapted to very low oxygen conditions. Above are some of the classic and extensive drawings of foraminifera made on stone by A. T. Hollick from sketches and specimens provided by Henry Bowman Brady following the dredging voyages of HMS Challenger during the 1870s. Shown are several specimens similar to foraminifera that live in low-oxygen environments: representatives of the genera Uvigerina (left) and Cassiduli- noides (center), from the southeastern Pacific; and Hoglündina, from the South Atlantic. found not only in fishes but also in duction. The youngest offspring live Community Life in an OMZ certain OMZ-dwelling bivalves, in- farther up the water column, and the Like communities of animals that oc- cluding mussels we saw on the mar- next life stage lives in the shallowest cupy different habitats on dry land, gin off Oman. part of the OMZ, where extraordinarily communities in undersea habitats also Copepods (tiny crustaceans that low oxygen concentrations (0.069 milli- differ in size and composition. The function like insects of the sea) in the liter per liter) protect them from preda- first scientist to study the unique fea- genus Lucicutia have fine-tuned their tors. The crustacean Orchomene obtusis, tures of OMZ communities in detail life cycles to different oxygen levels. L. which scavenges in the bottom waters was Howard Sanders of WHOI. Com- grandis, a large red-orange species, is of Saanich Inlet, British Columbia, paring fauna dredged from marine common in the most hostile regions of moves in and out of OMZs. It takes ad- and estuarine environments off the the Arabian Sea. Adults live at the vantage of the plentiful food and lack coasts of India, Madagascar, New Eng- deepest level of the OMZ, where the of predators in hypoxic waters and land and South America, he concluded oxygen concentration of about 0.14 swims out to obtain more oxygen—a in 1968 that two Arabian Sea samples milliliter per liter is adequate for repro- strategy dubbed “eat and run.” contained the fewest species. “The probable cause for these modest diversity values is the low-oxygen minimum layer found throughout the northern Arabian Sea at the 100 to 200 meter depth,” he wrote. Sampling across the continental margin off Walvis Bay on the Atlantic coast of the southern African country now called Namibia, Sanders noted even less diversity at 100 meters, where the oxygen saturation was below 2 percent. Around Walvis Bay, the existence of an OMZ is betrayed by the occasional smell of rotten eggs; the smell comes from sediments permeated with hydrogen sulfide. Figure 6. Although macrofauna are far less abundant than smaller organisms in the cen- Now that many OMZ communities ters of oxygen minimum zones, some genera have been studied, we can point to have adaptations that allow them to take ad- some common features. OMZs inter- vantage of the wealth of food in these regions sected by the seafloor tend to have of the ocean. The polychaete worm Prionos- populations of large, filamentous sul- pio has tentacle-like branchiae, which in- fur bacteria, such as the species de- crease its surface area, presumably enhanc- scribed above. Meiofauna (microscop- ing its ability to take up oxygen. It also builds ic animals) are also abundant in tubes out of sediment. Prionospio accounted OMZs, but there are limited numbers for two-thirds of the individual organisms in of macrofauna (animals larger than macrofauna retrieved from depths of 400 to 418 meters southwest of Masirah Island, half a millimeter) and megafauna Oman, where the oxygen concentration was (bigger animals, such as crabs, anem- 0.13 milliliter per liter. (Drawing and photo- ones and starfish). Biologists separate graph courtesy of Peter Lamont.) these groups by shaking their samples

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 440 American Scientist, Volume 90 with permission only. Contact [email protected]. through progressively smaller sieves. three percent of the particles were of an OMZ than in well-oxygenated re- Megafauna can be recognized with the smaller than 500 micrometers, com- gions of the ocean. The most abundant naked eye. pared with 66 percent of those from the members are annelids, which tolerate Small body size is one of the most 3,350-meter sample. However, the OMZ oxygen depletion well, perhaps because obvious features of animals in OMZs. samples yielded the foraminifera with their thin, bare bodies facilitate oxygen The barren appearance of Volcano 7’s the largest dimensions. In total, Gooday diffusion. These segmented worms, summit results not from the absence of counted only 70 different species of which tend to be surface feeders, are life but from the lack of animals larger foraminifera from the OMZ compared usually polychaetes, but sometimes than a centimeter. There appears to be with 366 species from the deeper site. oligochaetes (which have fewer ap- no simple relation between oxygen Structurally complex, thin-shelled pendages) can be dominant. Analyzing content and body size within any foraminifera called rotaliids, which are data from the eastern Pacific, northeast- group of small animals, however. very tolerant of low oxygen, dominated ern Atlantic and northwestern Arabian The single-celled organisms of the the OMZ samples but were uncommon Sea, John Gage of the Scottish Associa- order Foraminifera are important in the deep water. tion of Marine Sciences and I concluded members of OMZ communities. For- Nematode worms dominate the that the availability of both oxygen and aminifera tend to be more abundant meiofauna in OMZs, accounting for organic carbon determines the richness than multicellular animals of similar more than 95 percent of the organisms of macrofaunal species in OMZs until size, nematodes excepted. In contrast by number and by weight. These the oxygen content rises to about 0.45 with metazoans that have adapted to minute, simple animals inhabit dry milliliter per liter. Above that level, oxy- OMZs, foraminifera have calcareous land and fresh water as well as being gen is much less important. or agglutinated shells, called tests, the predominant multicellular animals Among the macrofauna, crustaceans which range in size from less than 0.1 in marine sediments. The large surface- and molluscs are rare where the oxygen to several centimeters. During a 1994 to-volume ratio of their narrow bodies concentration is below 0.15 milliliter per expedition, Andrew Gooday of the is eminently suited to efficient oxygen liter. Some exceptions are Ampelisca am- Southampton Oceanography Centre uptake. Thus, the density of nematodes phipods, which build parchment-like collected foraminifera from soupy mud can be several times greater at the core tubes in soft sediments, the gastropod under the OMZ off Oman. Lowering of an OMZ than in deeper, well-oxy- Astyris permodesta and a thin-shelled corers over the side of a British vessel, genated waters. Many other meiofau- mussel, Amygdalum anoxicolum, which the Royal Research Ship Discovery, he nal groups—copepods, kinorhynchs, builds a cocoon from mud. G. ingens can sampled both the center of the OMZ, at tardigrades and rotifers—are poorly live at oxygen concentrations as low as 412 meters, where the oxygen concen- represented in OMZ communities. 0.2 milliliter per liter. Megafauna—such tration was 0.13 milliliter per liter, and a Even so, meiofaunal density in OMZs as crabs and shrimp—are also rare in site at 3,350 meters, where it was about often matches that in densely populat- the heart of an OMZ, where oxygen 3 milliliters per liter. In the top centime- ed oxygenated regions, correlating pos- drops below 0.1 milliliter per liter. Be- ter of the cores, Gooday found 25 times itively with food availability or quality. low the core, where oxygen concentra- as many foraminifera in the OMZ sam- The density of macrofauna can be 30 tions are somewhat higher and nutri- ples as in the deeper samples. Ninety- percent to 99 percent lower in the core ents still plentiful, larger animals

Figure 7. Volcano 7’s summit lies in the core of an oxygen-minimum zone. Many shrimp and a rattail fish (Nezumia liolepis) are visible in the left-hand photograph, taken 250 meters below the top of the volcano, near the lower boundary of the oxygen-minimum zone. The sediments teem with microscopic foraminifera and nematode worms, which feed on detritus that sinks from the ocean’s productive surface layers. At right, closer to the summit, dense populations of galatheid crabs, along with sponges, can be seen. Oxygen concentrations here are lower, but food re- mains plentiful for organisms that tolerate the lack of oxygen. (Photographs courtesy of the author.)

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 2002 September–October 441 with permission only. Contact [email protected]. 750 and 770 meters, there were succes- phytoplanktonic organisms that obtain sive zones of crabs, shrimp, brittle their energy from the sun and with ani- stars and anemones, with very dense mals that eat phytoplankton; when patches of megafauna—as many as 19 these organisms die they sink as detri- animals per square meter—at 800 to tus. Because sinking detritus is so abun- 810 meters. Below 1,000 meters, where dant in oxygen-depleted waters, scien- the oxygen concentration was higher, tists used to assume that photosynthetic the density fell to 0.5 animals per organisms stood alone as the energy square meter. source forming the base of the food Such surveys illustrate another strik- chain in OMZs. Prompted by Victor ing feature of OMZ communities: re- Gallardo, we now wonder whether duced diversity. On the summit of Vol- chemosynthesis, practiced by sulfur cano 7, more than half the rotaliid bacteria, could also play a role. Figure 8. The sulfur-oxidizing bacterium Thioploca is common in sediments off cen- foraminifera collected belonged to a In 1994, Henrik Fossing of the Max tral and northern Chile, Peru, Oman, Namib- single species. The foraminiferan Epis- Planck Institute of Marine Microbiolo- ia and Pakistan. Aligned end-to-end, the tominella bradyana is dominant in Mexi- gy in Bremen, Victor Gallardo and in- large cells form filaments, which are bundled co’s Gulf of Tehuantepec, Nonionella vestigators from Denmark sampled inside slimy sheaths. (Photomicrograph cour- stella in the Santa Barbara Basin and sediment from the OMZ off Chile. After tesy of the author.) Bolivina seminuda on the Oman margin. squeezing pieces of Thioploca mat, they Likewise, the most abundant macro- measured nitrate concentrations. The become more common. Shrimp, crabs, faunal species can account for up to 83 first liquid to emerge had a nitrate con- sponges and brittle stars often congre- percent of the total macrofauna in an tent similar to that of seawater. But gate at such edges. The lower boundary OMZ. Although oxygen concentration greater pressure released liquid with of an OMZ is the region richest in appears to reduce diversity when it 100 times as much nitrate. Subsequent megafauna; it can also be one of the falls below 0.4 to 0.3 milliliter per liter, studies showed that this liquid came richest habitats in the ocean. it is not the sole factor. Toxic sulfides from the membrane-bound vacuole that A photographic transect down Vol- or competitive interactions might also occupies most of the bacterium. Aston- cano 7, which lies within an OMZ from contribute to low diversity in OMZs. ishingly, the nitrate concentration in its summit to a depth of 1,300 meters, such vacuoles was 500 millimolar—up showed only bony fish called rattails, Tracing the Food Chain to 20,000 times the concentration in sea- sponges and seapens at 740 meters, Animals in OMZs obtain energy and water. Thus, Thioploca stores the nitrate where the water contained less than 0.1 carbon for growth by breaking down it needs for oxidizing hydrogen sulfide. milliliter of oxygen per liter. Between detritus. Surface waters are filled with The nitrate takes the place of the oxygen used by most organisms, and the vacuole serves as a lung. Presumably, organic CO carbon 2 the ability to store nitrate gives Thioploca a distinct advantage over bacteria that must have simultaneous access to an nitrate oxidant and a reduced compound. Hydrogen sulfide, the reduced compound used by Thioploca, is produced by sedimentary bacteria that reduce sulfate. In some locations, filaments of the sulfate-reducing Desulfonema orna- ment the sheath of Thioploca, creating an efficient recycling system. A more intimate arrangement has evolved in the gutless oligochaete Olavius algar- Figure 9. Filaments glide down from mats of 5 centimeters vensis, which shelters two bacterial Thioploca to obtain hydrogen sulfide (H2S), moving through sediment at rates of up to 1 species in its cells. One bacterium pro- centimeter per hour. Sedimentary bacteria that duces sulfide, and the other oxidizes 2– reduce sulfate (SO4 ) generate the hydrogen this product. Even in sediments com- sulfide. Thioploca oxidizes the sulfide with ni- pletely devoid of oxygen, hydrogen – trate (NO3 ), forming nitrogen, sulfur and wa- sulfide is consumed rapidly. Thus, bac- ter. This reaction releases energy for growth teria in anoxic sediments reduce sul- and reproduction. The nitrate comes from the fate to hydrogen sulfide. Whereas bacterium’s large central vacuole, where it is some sulfur-oxidizing bacteria require highly concentrated. Thioploca collects nitrate oxygen to oxidize hydrogen sulfide, hydrogen by gliding up into seawater. The sulfur liberat- sulfide ed from the oxidation of hydrogen sulfide ac- others use nitrate, releasing energy that cumulates as shiny globules in the bacterium’s can be used for growth. These bacteria cytoplasm. (Reconstruction courtesy of Heide can be free-living, as is Thioploca, or Schulz, University of California, Davis; draw- they may live as symbionts, as do Olav- 2.5 centimeters ing adapted from Fossing et al. 1995.) ius and bivalves of the family Lu-

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 442 American Scientist, Volume 90 with permission only. Contact [email protected]. cinidae. When seafloor bacteria are di- 0 oxic gested by other organisms, the energy 0.2 and carbon stored in their cells be- site 893 comes available once more. Therefore, 0.4 dysoxicdy chemosynthesis as well as photosyn- 0.6 thesis might initiate food chains that microxicmi 0.8 support OMZ animals. One of our dysoxicdy xic goals for the next few years is to assess 1.0 the extent to which chemosynthesis fu- depth (kilometers) 1.2 site els oxygen-minimum ecosystems. a b 1017 c 1.4 The Global Climate Connection 0123456 One of the advantages of studying dissolved oxygen (milliliters per liter of seawater) OMZs is their stability, which permits Figure 10. By studying the relations of modern foraminifera to oxygen concentrations—here observations over extended periods. using sedimentary cores from Ocean Drilling Program sites 893 and 1017—scientists can esti- But although OMZs persist for thou- mate the oxygen conditions that prevailed when fossilized foraminifera were alive. Kevin sands of years, they do expand and Cannariato and James Kennett at the University of California, Santa Barbara, estimated that contract as the global climate changes. the oxygen-minimum zone that lies along the northeastern Pacific margin (a; OMZ shown in Detecting and understanding prior al- dark blue) expanded during interstadials (warm periods between glacial advances) 16/17, 14, terations might help us predict—or 11, 8, Bølling-Allerod and earliest Holocene (b).The zone shrank, hypothetically, during icy even delay—future changes. cold periods (c). If OMZs expanded during warm periods of Earth’s history, global warming is Climatic changes likely to have af- likely to trigger future expansions. (Adapted from Cannariato and Kennett 1999.) fected the oceans’ oxygen inventory in- 800 clude the ice ages. These periods have not been unremittingly cold: Ice cores Antarctic North Atlantic from Greenland reveal that at least 24 surface water periods of sudden warming occurred 700 between 115,000 and 14,000 years ago. other oceans These interstadials—warm periods between icy cold periods—took no more than a few decades to develop, and 600 they persisted from decades to hundreds of years. Given the impossibility of measur- 500 ing the oxygen content of past waters, scientists have had to devise proxy methods. One method records the number and species of fossilized 400 North Atlantic foraminifera in samples of ocean sedi- Deep Water ment. Identifying the foraminifera that * (moles per 100 grams) currently dominate waters with known 2 O oxygen concentrations allows us to in- 300 fer the concentrations that existed when the fossilized foraminifera were O2 solubility alive. Using this approach, Kevin Can- 200 nariato and James Kennett at the Uni- versity of California, Santa Barbara, recently made detailed studies of the Santa Lucia Slope, about 60 kilometers 100 west of Point Conception, California. –5 0 5 10 15 20 25 30 35 After seeing how assemblages of fos- potential temperature (Celsius) silized foraminifera changed over the past 60,000 years, they determined Figure 11. At the Scripps Institution of Oceanography, Ralph Keeling and Hernán Garcia made whether the major changes correlated a scatter plot of O2* against temperature. O2* represents the amount of oxygen a body of seawa- with alterations in global climate. ter would lose to air or gain from air at a given temperature. Between 6 and 18 degrees Celsius, The foraminifera Bolivina argentea, O2* correlated strongly with potential temperature (water temperature corrected for the adiabat- Buliminella tenuata and Chilostomella ic heating associated with depth). Thus, as seawater warms, as it does in the low latitudes, it los- ovoidea currently dominate the Santa es oxygen; as it cools in higher latitudes, it takes oxygen from the air. The most striking feature of the scatter plot is the slope, which is much steeper than the plot of oxygen solubility against tem- Lucia slope where oxygen concentra- perature (dashed black line). This reveals that biological activities as well as oxygen solubility de- tions are between 0.1 and 0.3 milliliter termine how much oxygen an ocean loses or gains as temperature rises or falls. Keeling and Gar- per liter. Different foraminifera are cia used this relation between oxygen flux and temperature to estimate the amount of outgassing dominant where oxygen concentra- that took place as seawater temperatures rose during the 1990s. (Adapted from Keeling and Gar- tions are higher. The fossil study cia 2002, by permission of the National Academy of Sciences.)

© 2002 Sigma Xi, The Scientific Research Society. Reproduction 2002 September–October 443 with permission only. Contact [email protected]. showed that past assemblages changed sity at OMZ boundaries. Molecular, en- ships between oxygen, organic matter and rapidly. Foraminifera typical of low zymatic, physiologic and reproductive the diversity of bathyal macrofauna. Deep- oxygen concentrations were dominant studies together will allow us to solve Sea Research II 45:129–163. during warm periods such as the inter- the puzzle of how animals survive at Levin, L. A., J. Gage, P. Lamont, L. Cammidge, C. Martin, A. Patience and J. Crooks. 1997. stadials and the last glacial maximum, such low oxygen concentrations. The Infaunal community structure in a low-oxy- whereas foraminifera typical of higher role of chemosynthesis in oxygen-de- gen, organic-rich habitat on the Oman con- oxygen concentrations were dominant pleted zones and the contributions of tinental slope, NW Arabian Sea. In Respons- during the cold periods. The California OMZs to the generation of new species es of Marine Organisms to Their Environments; Proceedings of the 30th European Marine Bio- OMZ presumably expanded into shal- are among the most exciting evolution- logical Symposium, eds. L. Hawkins and S. lower and deeper waters during cer- ary questions. By integrating biogeo- Hutchinson. Southampton, U.K.: University tain warm periods and contracted dur- chemical, molecular, microbiological of Southampton, pp. 223–230. ing cold periods. Such fluctuations and ecological research, scientists hope Levin, L. A., J. D. Gage, C. Martin and P. A. La- over time appear to have been com- to fill in some of the gaps. Given the mont. 2000. Macrobenthic community struc- mon along the northeastern Pacific unique features of OMZs, their findings ture within and beneath the oxygen minimum zone, NW Arabian Sea. Deep-Sea margin and northern Arabian Sea. could be surprising. Research II 47:189–226. Because history tends to repeat itself, Levin, L. A., C. L. Huggett and K. F. Wishner. the current trend toward global warm- Bibliography 1991. Control of deep-sea benthic communi- ing has the potential to expand OMZs, ty structure by oxygen and organic-matter Cannariato, K. G., and J. P. Kennett. 1999. Cli- depriving large regions of the ocean of gradients in the eastern Pacific Ocean. Jour- matically related millennial-scale fluctua- nal of Marine Research 49:763–800. commercially useful fauna. Computer tions in strength of California margin oxy- modeling completed this spring by gen-minimum zone during the past 60 k.y. Neira, C., J. Sellanes, L. A. Levin and W. E. Geology 27:975–978. Arntz, 2001. Meiofaunal distributions on the Ralph Keeling and Hernán Garcia, two Peru margin: Relationship to oxygen and colleagues at Scripps, suggests that the Childress, J. J. 1975. The respiratory rates of organic matter availability. Deep-Sea Research midwater crustaceans as a function of depth I 48:2453–2472. oceanic inventory of oxygen is already occurrence and relation to the oxygen mini- falling. The scientists plotted a measure mum layer off Southern California. Compar- Sanders, H. L. 1968. Marine benthic diversity: of the amount of oxygen that various ative Biochemistry and Physiology 50A: A comparative study. The American Natural- ist 102:243–282. oceans would lose to the atmosphere 787–799. Childress, J. J., and B. A. Seibel. 1998. Life at sta- Sanders, H. L. 1969. Benthic marine diversity as water temperature rose. The result- and the stability-time hypothesis. In Diversity ing slope was several times steeper ble low oxygen levels: Adaptations of animals to oceanic oxygen minimal layers. The and Stability in Ecological Systems, eds. G. M. than a plot of oxygen solubility against Journal of Experimental Biology 201:1223–1232. Woodwell and H. H. Smith. Upton, NY: Brookhaven National Laboratory, pp. 71–81. temperature. Thus, the influx of detri- Cook, A. A., P. J. D. Lambshead, L. E. Hawkins, Sanders, N. K., and J. J. Childress. 1990. Adap- tus into the ocean’s interior, not oxy- N. Mitchell and L. A. Levin. 2000. Nema- tations to the deep-sea oxygen minimum gen solubility, must be the major influ- tode abundance at the oxygen minimum layer: Binding to the hemocyanin of the ba- zone in the Arabian Sea. Deep-Sea Research II ence on oxygen exchange. The relation thypelagic mysid, Gnathophausia ingens 47:75–85. between oxygen exchange and heating Dohrn. The Biological Bulletin 178:286–294. Diaz, R. J., and R. Rosenberg. 1995. Marine allowed Keeling and Garcia to estimate Schulz, H. N., T. Brinkhoff, T. G. Ferdelman, benthic hypoxia: A review of its ecological M. Hernández Mariné, A. Teske and B. B. oxygen loss from the world’s oceans for effects and the behavioral responses of ben- Jørgensen. 1999. Dense populations of a gi- the years 1990 to 2000. The figure they thic macrofauna. Oceanography and Marine ant sulfur bacterium in Namibian shelf sed- Biology: an Annual Review 33:245–303. derived was 2.9 trillion moles of oxy- iments. Science 284:493–495. Fossing, H., V. A. Gallardo, B. B. Jørgensen, M. gen per year. To obtain this amount, Wishner, K. F., C. J. Ashjian, C. Gelfman, M. Hüttel, L. P. Nielsen, H. Schulz, D. E. Can- you would have to remove all the oxy- Gowing, L. Kann, L. A. Levin, L. S. Mul- field, S. Forster, R. N. Glud, J. K. Gunder- gen from 92 trillion kiloliters of surface lineaux and J. Saltzman. 1995. Pelagic and sen, J. Küver, N. B. Ramsing, A. Teske, B. benthic ecology of the lower interface of the seawater at 5 degrees Celsius (about Thamdrup and O. Ulloa. 1995. Concentra- Eastern Tropical Pacific oxygen minimum one ten-thousandth of the oxygen in tion and transport of nitrate by the mat- zone. Deep-Sea Research I 42:93–115. all the world’s oceans). The calcula- forming sulphur bacterium Thioploca. Nature 374:713–715. Wishner, K. F., M. M. Gowing and C. Gelfman. tions suggested that 18 percent of the 2000. Living in suboxia: Ecology of an Ara- lost oxygen came from the North At- Gooday, A. J., J. M. Bernhard, L. A. Levin and bian Sea oxygen minimum copepod. Lim- lantic, 20 percent from the deep S. B. Suhr. 2000. Foraminifera in the Arabian nology and Oceanography 45:1576–1593. Sea oxygen minimum zone and other oxy- Southern Ocean and 61 percent from gen-deficient settings: Taxonomic composi- Wishner, K., L. Levin, M. Gowing and L. the rest of the upper ocean. The global tion, diversity, and relation to metazoan fau- Mullineaux. 1990. Involvement of the oxy- estimate is not dissimilar to that de- nas. Deep-Sea Research II 47:25–54. gen minimum in benthic zonation on a deep seamount. Nature 346:57–59. rived using ocean general circulation Jørgensen, B. B., and V. A. Gallardo. 1999. Thio- models, and oxygen loss is likely to ploca spp.: Filamentous sulfur bacteria with increase as human activities exacer- nitrate vacuoles. FEMS Microbiology Ecology 28:301–313. Links to Internet resources for further bate global warming. Keeling, R. F., and H. E. Garcia. 2002. The exploration of “Deep-Ocean Life Where To test these models and predict the change in oceanic O inventory associated 2 Oxygen Is Scarce” are available on the impact of global warming on marine with recent global warming. Proceedings of fauna and our seafood supply, it will the National Academy of Sciences of the U.S.A. American Scientist Web site: be necessary to directly monitor the 99:7848–7853. changing oxygen content of the world’s Levin, L. A. In press. Oxygen minimum zone http://www.americanscientist.org/ benthos: Adaptation and community re- articles/02articles/levin.html oceans. To learn more about OMZs, we sponses to hypoxia. Oceanography and Ma- will need to identify factors that con- rine Biology: an Annual Review. trol animal abundance and boost den- Levin, L. A., and J. D. Gage. 1998. Relation-