J Anthony Koslow. American Scientist. Volume 85, Issue 2. Mar/Apr 1997.
In the early 19th century, when the waters of the ocean were first sampled at depth, scientists generally believed that the deep ocean was lifeless. But like many scientific theories that have come and gone, this one merely revealed the limits of observation. In the course of the great Challenger Expedition of 1872-76, more than 1,500 species were retrieved from ocean depths below 1,000 meters.
Since that time, the immense variety of life forms in the deep sea has been a source of public and scientific fascination. Unusual and sometimes bizarre creatures greet deep-sea explorers. These fish-termed bathypelagic because they inhabit the water column at depths below approximately 1,000 meters-provide hints that although life at depth is not impossible, it may require many adaptations. Most notably, deep-sea fish generally have greatly reduced bone and musculature, facilitating maintenance of neutral buoyancy. With a low protein and fat content and high proportions of water in their body tissue, they are not likely to turn up on the dinner plate.
Unlike the firm-bodied fish that are commonly encountered in shallow water and are adapted for rapid movement or sustained cruising, many bathypelagic fishes are eel-like, maintaining a minimal profile while moving sinuously through the water seeking prey Others, such as the anglerfish, are somewhat blob-like and drift with ambient currents. Rather than actively searching, many bathypelagic predators use lures to attract their prey and have extensible jaws and large stomachs so they may gulp down other relatively weak creatures almost as large as themselves.
The physiology of bathypelagic fishes is also adapted to life in the deep sea. Measurements indicate that their metabolic levels are 1 percent to 10 percent of those of fishes that live in nearsurface waters or migrate from daytime depths of several hundred meters to feed at night near the surface.
These few observations suggest that fundamental modifications in body plan, bodily composition and metabolism are required for life in the deep sea. Until recently it was believed that these modifications were largely a response to low food availability. In the ocean, the biological activity called primary production-the growth of the microscopic plants (phytoplankton) that capture solar energy and form the beginning of the food chain-is largely confined to the upper 100 meters of the water column, where there is adequate light for photosynthesis. Most phytoplankton are consumed and recycled in this near-surface layer, so the abundance of zooplankton, the tiny animals that eat the algae, and of higher predators, such as fish and squid, declines exponentially with depth through the water column. Scarcity of resources in the deep led to the evolution of an energy-efficient way of life, it was hypothesized.
However, recent research by Jim Childress of the University of California, Santa Barbara, and coworkers has indicated that reduced metabolism in the deep sea is more likely a response to reduced light at these depths than simply a consequence of a lack of prey (Childress et al. 1980). They argue that in an open-water environment where there is reasonable ambient light, visually orienting animals protect themselves by maintaining adequate distance from predators.
In the deep sea, where there is virtually no ambient light, reaction distances are much reduced, and there is no advantage to maintaining strong burst swimming capability. The smaller midwater fishes have adopted a highly energy-efficient ecological strategy. By drastically reducing their locomotory capacity and associated metabolic costs, these fishes are able to maintain high growth rates in a resource-poor environment. Maintenance of high growth indicates that reduced metabolism in these fishes is not simply a response to extreme, lowfood conditions. In support of their argument, Childress and his colleagues also show that unlike most bathypelagic fish, animals that do not visually orient, such as certain crustaceans and gelatinous zooplankton, do not show a significant decline in metabolism with depth.
This provocative hypothesis may explain many aspects of deep-sea ecology but does not seem to apply to a group of deep-sea fishes that were poorly known (even by the standards of deepsea biology) until discovery of their commercial potential brought them to the forefront of deep-sea research. A decade or two ago, it was considered highly unlikely that significant commercial fisheries would ever develop below approximately 500 meters in depth, because of the scarcity of life at those depths and its poor palatability. Then in the 1980s, fisheries for orange roughy (Hoplostethus atlanticus) and deepwater oreos (Family Oreosomatidae) developed at 700-1,400 meters on the deep plateaus and seamounts around New Zealand and southeastern Australia. These operations have become among the largest and most valuable fisheries in these countries, with over half a million metric tons landed since that time.
The viability of these fisheries depends on the fishes’ good flesh quality their high protein and lipid content and low water content-and their tendency to maintain themselves in substantial aggregations around fixed deep-sea features, such as seamounts, rather than being spread out in low densities over vast expanses of the deep sea.
These observations suggest that deepwater fisheries are based on a group of species that differ fundamentally from those generally considered typical of the deep-sea enviromnent. In this article, I explore what has been learned about the energetics of these species and how these massive aggregations support themselves in the deep-sea environment; how their metabolism and energetics compare with that of other deepwater species and of near-surface dwelling fishes; how these substantial aggregations support themselves in the deep sea-in particular, whether there are significant energetic pathways to the deep sea other than the sparse rain of detritus from the surface.
A Fish of a Different Color
What evidence is there that the seamount-associated fishes differ fundamentally from others in the deep sea? The first indication, as suggested above, is the firm flesh of orange roughy and other commercial deep-sea species, based upon their high protein and low water content. Childress and coworkers showed that the bodily composition of fishes, in particular their protein content, is correlated with metabolic level, such that fishes with poor musculature (watery, poor-quality flesh) and hence low protein content maintain low metabolic levels. Active fishes with high metabolic rates require good musculature and therefore have high protein levels in their flesh.
My colleagues and I used two methods to estimate the energy budget of orange roughy. First we estimated its food intake with an extensive field study of its feeding, which provided information on average stomach fullness and digestion rate (Bulman and Koslow 1992). Knowing the orange roughy’s average daily ration (about 1 percent of body weight) and annual growth and reproductive output, we could estimate its mean metabolic expenditure by difference. A second method involved an assay of the metabolically active enzyme lactate dehydrogenase (LDH), the concentration of which has been shown to be closely correlated with respiration rate.
Both these methods indicate that although the orange roughy does not diurnally migrate into near-surface waters, its metabolism is substantially higher than that of bathypelagic nonmigratory species and of deepwater species dispersed over the flat seafloor. In comparing the metabolism of orange roughy, which weighs as an adult an average of 1.5 kilograms, and deepwater pelagic species, which typically weigh several grams, metabolic rates must be scaled for size because metabolism generally increases with body weight by an exponent of approximately 0.75. As a result, orange roughy mass-specific metabolism, which initially appears to be comparable to that of mesopelagic fishes that conduct extensive daily vertical migrations, is in fact substantially higher when scaled to a common body size (Figure 4). Indeed its metabolism seems comparable to that of the haddock, a demersal species living on the continental shelf at depths of less than 200 meters, a major exception to the general rule of declining metabolism with depth (Koslow 1996).
The high metabolism of orange roughy has considerable implications for its energetic efficiency The reduced metabolism of most other deepwater fishes leads to their having exceptionally efficient growth-growth efficiencies of between 25 and 50 percent-despite the limited food available to them (see Figure 5). The growth and reproductive efficiency of orange roughy, on the other hand, is on the order of only 5 percent, because virtually all its food energy is consumed by activity
The orange roughy’s popularity with fishermen derives not only from its firm flesh but also from its behavior. Like the cardinalfish but unlike most deepwater species, orange roughy are not found widely dispersed in open water or over the bottom. Rather, the fish maintain themselves in substantial aggregations around distinct topographic features, such as seamounts, despite the relatively strong currents that often prevail in these environments. During the early days of the orange roughy fishery, catch rates during a trawl’s time on the bottom often exceeded 10 metric tons per minute.
The orange roughy’s choice of a seamount habitat has an obvious connection with its metabolic characteristics. Extending several hundred meters or more from the seafloor, seamounts have complex effects on deep-ocean circulation, much as mountains affect the wind field around them. Currents are on the order of 10 to 40 centimeters per second in the vicinity of a seamount, and may be enhanced over particular portions. Simply to maintain itself in the vicinity of a seamount requires that a fish make a significant metabolic expenditure. There may also be eddy-like features in the lee of seamounts or over their summit, and one might speculate that fish aggregations tend to form in these energetically quiescent areas, much as trout maintain themselves in the back eddies of a stream.
Our research team got an indication of the swimming abilities of orange roughy when we attempted to photograph them. Entire aggregations dispersed rapidly when the camera system being lowered was still about 130 meters above them. These observations were made with an acoustic system mounted on the hull of the research vessel. The acoustic beam at the depths of these observations-800-1,000 metershas a radius of 30 to 40 meters, so the aggregations dispersed at least this distance. In contrast, submersibles have approached deepwater species with low metabolic levels sufficiently closely to be able to coax them into respirometry chambers (Smith and Brown 1983).
Stretching the Food Web
The orange roughy, then, has characteristics that challenge the conventional models of energy supply to the deep sea. We re-evaluated these models by studying the food web underlying production of orange roughy off southeastern Australia.
From examining fishing records and surveys, biologists can get fairly good estimates of how many fish are in the water. Before fishing began, the orange roughy population around southeastern Australia is thought to have totaled approximately 200,000 metric tons. This estimate is derived from acoustic and egg surveys and the record of the accumulated catch, which to date totals 158,000 tons.
The stock lives in the relatively narrow midslope region between the depths of 700 and 1,200 meters off southeastern Australia, an overall area of about 4,000 square kilometers. However, when spawning is not going on, it is concentrated predominantly around seamounts located off southern Tasmania, an area of only 1,200 square kilometers. A trawl survey of the region that excluded these seamounts by sampling only on flat, readily trawled ocean bottom accounted for only 15,000 of the estimated 200,000 tons of orange roughy
The density of orange roughy biomass in the water column is therefore on the order of 50-125 grams of wet weight per square meter. (Biomass is customarily measured as the amount of material in a square-meter cross section of the water column.) By assuming that the mass of carbon in the biomass is 5 percent of the fish’s wet weight, we can estimate that the orange roughy biomass amounts to 2.5-6.25 grams of carbon per square meter, the choice of higher or lower number depending on whether the biomass is compared to the larger or smaller area.
It is interesting to compare the density of an aggregating species, such as orange roughy, with the density of nonaggregating species living either over the seafloor or within the water column. The density of all fish, including orange roughy, was estimated at only 4.8 grams of wet weight per square meter on flat ground at mid-slope depth, following a trawl survey carried out on the readily trawled ground around southeastern Australia in 1988-89. This is only 4 to 10 percent of the density of aggregated orange roughy alone. Another study indicated that the biomass of all nekton (fish, squid and large crustaceans) throughout the water column at 1,000 meters depth was 6 grams per square meter, as measured with a small midwater trawl (mouth area 105 square meters), and between 50 and 150 grams of wet weight per square meter, measured acoustically. (The acoustic estimate is probably more realistic, because many fish avoid midwater nets.)
The density of orange roughy around the seamounts may therefore be considered to be an order of magnitude larger than the density of nonaggregated demersal fish (fish that are not free-swimming but stay along the seafloor) and probably of the same order as the abundance of all nekton throughout the water column.
Orange roughy feed at the fourthplus trophic level: They primarily consume small fish and squid, which in turn prey on small crustaceans. To the extent that these crustaceans feed as herbivores on the primary plant production near the surface and are linked to the orange roughy through a series of vertical migrations, the roughy may be considered to be at the fourth trophic level. However, to the extent that the crustaceans feed on detritus falling out of the near-surface layer-fecal pellets, molted exoskeletons and so on-they are feeding at a trophic level higher on the food chain. Also, some of the orange roughy’s prey in turn prey on small fishes, which again adds a step to the trophic web. Placing the orange roughy at the fourth trophic level is therefore conservative.
A simple food-chain calculation indicates that in situ primary production is insufficient to meet the energy requirements of the aggregated orange roughy. As I did above, I shall use an ecological accounting method that uses grams of carbon per square meter of water column to represent the biomass produced at each trophic level and consumed at the next.
Net primary production in the region is approximately 200 grams of carbon per square meter per year. The efficiency with which this production is transferred up the food chain, called ecological efficiency, is the ratio of the energy consumed to the energy supplied. In some parts of the sea this is as high as 20 percent, but in the area studied it is typically around 10 percent.
Therefore, one can estimate that the amount of carbon available to the second trophic level in the region is 20 grams, and approximately 2 grams of carbon per square meter is produced annually by the third trophic level and potentially available to the orange roughy. It is only 0.2 grams if one assumes an additional link in the food chain.
However, if we assume that the density of orange roughy on their feeding ground is 5 grams of carbon per square meter and that they ingest 1 percent of their body weight daily (the best estimate from the feeding study around southeastern Australia), then they require approximately 18 grams of carbon per square meter-10 times what this simple calculation indicates is available.
Kinks in the Food Chain
My calculation assumes that the food web is integrated throughout the water column. In fact things are not so simple. Only a fraction of the surface production is available to a species, such as the orange roughy, that resides at mid-slope depth. Food from the surface reaches the interior of the ocean by two mechanisms: sedimentation and vertical migration (see Figure 6).
Sedimentation refers to the sinking of ungrazed phytoplankton, fecal pellets, crustacean molts and other detritus from the surface to deeper waters. Vertical migration refers to the fact that many marine species reside between several hundred and 1,000 meters depth during the day to avoid visually orienting predators, and migrate to near-surface waters to feed at night. Some zooplankton species also estivate, or linger in a dormant state, at depth during the unproductive winter months, returning to the surface to reproduce and feed in spring. These contributions to the deepwater ecosystem off southeastern Australia can now be estimated.
Sediment traps deployed in our study off southeastern Australia indicated that, of the 200 grams of carbon per square meter annual net primary production at the surface, 15 grams sedimented to depths greater than 650 meters. This material can be considered as production at the base of the food chain provided to the midwater community, although it is nutritionally somewhat inferior. Using the 10-percent rule of thumb for ecological efficiency, the sedimented material provides approximately 0.15 grams of carbon per square meter to the fourth trophic level.
Many of the dominant zooplankton species carry out a seasonal migration, descending to 1,000 meters during the less productive time of year. The difference between the biomass of the zooplankton at depth at the beginning and the end of the estivation period indicates that this mechanism accounted for approximately 1 gram of carbon per square meter being transported annually from the surface and consumed at depths below 500 meters. These zooplankton presumably were consumed by the small midwater plankton-feeders, which are fed on by the orange roughy. Given the assumption of 10 percent efficiency again, seasonal plankton migrations accounted for another 0.1 gram of production per square meter by the third trophic level.
About 50 percent of the small fishes and squids sampled with a midwater trawl net carried out daily migrations from depths below 500 meters to the water above this depth. Some of these migrators are preyed on when they are in the near-surface layer, and some are consumed at depth. If 50 percent of the production of this migratory community were consumed below 500 meters, this would result in an annual flux to the deep water of approximately 1 gram of carbon per square meter per year.
The annualized contributions of the particle flux from the surface and of diurnal and seasonal migrators to the fourth trophic level total 1.25 grams of carbon. Interestingly, this result is similar to the result of our initial calculation based solely on an estimate of primary production and an estimate of 10 percent ecological efficiency between trophic levels.
Although this amount would satisfy less than 10 percent of the energetic requirements of the aggregated orange roughy, it does seem in balance with the energy requirements of nonaggregated midwater and demersal fishes. The nonmigratory midwater planktivores require an estimated 3 grams of carbon annually, which is similar to the estimated production of 2.5 grams per square meter from midwater zooplankton. Their food requirement is substantially less than that of the migratory midwater planktivores, despite their similar biomass, because as nonmigrators they have a lower metabolism. They also have less than half the carbon content of active migratory fishes as a result of their low protein and lipid content.
The density of nonaggregated demersal species in the water column prior to the onset of intensive fishing was just under 5 grams of wet weight, or 0.25 grams of carbon, per square meter. These fishes appear to have both very low metabolic rates (Figure 4) and very low growth (Figure 5), so their food consumption may be an order of magnitude lower than that of pelagic or seamount-associated fishes: approximately 0.15 percent of their body weight per day, or 0.14 grams of carbon per square meter annually, which is comparable to our estimate of production from the third trophic level (0.25 grams of carbon per year). These trophic calculations are even more approximate for these demersal fishes, because they feed at several trophic levels-although many, like the orange roughy, are higher predators, some are plankton-feeders and still others are scavengers or feed on benthic (or bottom) fauna that are supported by the rain of detritus from surface waters.
The commercial concentrations of orange roughy, however, simply cannot be sustained by biological production in the sunlit surface waters directly above them. Rather, they must depend on the flow of organisms past the seamounts where the roughy aggregate.
Dining at the Seamount Cafe
The orange roughy and oreos are not the only deep-sea fishes that require alternafive explanations for their survival. A recent review of the biology of seamounts listed approximately 75 species of fishes and invertebrates that are fished commercially from seamounts (Rogers 1994). Seamount summits range in depth from just a few tens of meters to more than 1,000 meters beneath the surface, so that the depth at which fishing takes place varies widely. Many of these fisheries are based on large, localized fish aggregations that clearly depend on imported food supplies to be sustained. It may be that, in discussing their ecology, all these fishes should be considered seamount aggregators rather than deep-sea dwellers. No matter what depth they inhabit, they may have more in common with other species fished from seamounts than with the fish living around them.
Why do so many species take up residence around seamounts? There is some evidence of localized upwelling and eddies around seamounts, which may enhance primary productivity near the surface. It is unlikely, however, that water could be retained around a seamount sufficiently long for enhanced primary production to work its way through the food web to the higher-trophic-level fish residing on the seamount itself.
John Isaacs and Richard Schwartzlose of the Scripps Institution of Oceanography were the first to observe that vertical migrators may be intercepted and hence concentrated by seamounts; these physically enhanced prey concentrations may serve to attract and support the predators seen aggregating on such features. As noted previously, the eddies formed by currents as they move over and around seamounts may also serve as backwaters, reducing the energetic cost associated with maintaining position around these topographic features.
There are interesting commonalities in the life history and energetics of species that aggregate around seamounts. Several are characterized by exceptional longevity. Orange roughy and at least two of the oreosomatids live to well over 100 years, and several Sebastes species live to more than 75 years. In these exceptionally long-lived fishes, growth and growth efficiency are exceedingly low. Their longevity is presumably linked to the scarcity of large predators in the deep sea, as well as to their mobility and sensitivity, which enables them to avoid predators, as well as camera systems!
However, aggregations of seamount fishes appear to subsist very near the margin of energetic sustainability. When the orange roughy off southeast Australia were first fished, only half of the adult females developed mature ovaries and spawned each year. When the population had been fished down to half its original biomass, the proportion rose to 75 percent. This response to reduced population size indicates that the reproductive output had been strongly limited by competition for food within aggregations.
The pelagic armorhead (Pseudopentaceros wheeleri), the subject of one of the first and largest of the seamount fisheries, may offer a more extreme example of energetic marginality. Between 1967 and 1975, by which time the seamounts were depleted of their fish resources, approximately a million tons of pelagic armorhead were fished by Soviet and Japanese trawlers on the southern Emperor and northern Hawaiian Ridge seamounts in the North Pacific.
The initial standing stock of pelagic armorhead was estimated at nearly 400,000 metric tons. Acoustic soundings from this fishery, like those of orange roughy aggregations, showed plumes of fish rising more than 100 meters into the water column above the seamount. The Soviet fishery scientist V B. Tseitlin carried out simple calculations to show how the armorhead aggregations could only be sustained by feeding on prey carried past the seamount on water currents.
The pelagic armorhead’s life history appears to have evolved so that the young spend the first 1-1/2 to 2-1/2 years of their life in near-surface waters, where they build up extremely large fat reserves. The fish then takes up residence on a seamount for the remaining 3-4 years of its life, during which time these fat reserves are gradually used up. The morphological difference between the “fat” and “lean” phases of the fish is so considerable that they were originally described as two distinct species!
The patterns of life history and energetics exhibited by seamount-aggregated species are in marked contrast to those of most bathypelagic species. Maintaining as they do a low-energy existence, many bathypelagic species are able to achieve fairly rapid, highly efficient growth, despite their relatively low food consumption. There is also no evidence that bathypelagic species exhibit a similar tendency toward marked longevity.
Seamount Fishes and Fisheries
There appears to be a distinct guild of fish species that aggregate around seamounts and that differ markedly from other deepwater species in their relatively high levels of food consumption and energy expenditure, low growth and a robust bodily composition and body plan suited for strong swimming performance. Many are characterized by extreme longevity. In general these aggregations seem to subsist upon a movable feast of meso- and bathypelagic organisms that drift past seamounts with the ambient current.
Their extremely low productivity combined with a habit of maintaining themselves in highly localized aggregations has made this group exceptionally susceptible to overfishing. This situation is aggravated by the fact that many seamounts are in international waters, where there is no management. Even for seamount fisheries within areas of national jurisdiction, the experience of the past few decades in New Zealand, the United States and Australia has been that they are typically depleted within 5-10 years, in the absence of a vigorous program of research and management.
Seamount fisheries take advantage of the fact that there is a group of species uniquely adapted to accreting the production of some of the least fertile waters of the world ocean-the deepwater and open-ocean realms. Science is only beginning to appreciate the ecology of these communities and the broad range of their behavioral and physiological adaptations to this environment. It is crucial that exploitation of seamount communities in the future is carried out sustainably. This will require gradual, controlled development of the fisheries so they do not outpace the development of a scientific basis for managing the resource. Their longevity and peculiar ecology means that many seamount populations, once depleted, will likely require decades, if not centuries, to regenerate.