Life in the Open Ocean. Joseph J. Torres

must accommodate the colder temperatures, higher pressures, lower light levels, and, sometimes, lower oxygen levels of the mid‐depths within their suite of adapted characters. A fascinating consequence of the changing environment with depth is the metabolic response of many deep‐living species to the change: metabolic rate declines precipitously with species’ depth of occurrence. It far exceeds that which would be predicted by the changes in the physical environment alone.

Figure 2.27 Relationship between routine respiration (solid line) and maximum respiration (dashed line) for groups of fishes with different minimum depths of occurrence.

      Source: Adapted from Torres et al. (1979), figure 1 (p. 190). Reproduced with the permission of Elsevier.

Childress (1971) was the first to report an unusually large decline in metabolism with depth in micronektonic species inhabiting the upper 1300 m of the water column off the coast of California, a cold temperate system. He found that species living at depths between 900 and 1300 m had a metabolic rate about 10% of those living in the upper 400 m when measured at the same temperature. The work suggested fundamental differences in the metabolic characteristics of the fauna living in different depth strata.

      Nearly forty years later, with investigations spanning the Atlantic, Pacific, Gulf of California, Gulf of Mexico, and Southern Ocean, and using a wide variety of different taxa, the trend has been found to be universal among many taxa. We now know a lot more about the decline in metabolism with depth, and a well‐accepted theory of why it occurs has been established.

The first taxa to be studied in detail for trends in metabolism vs. depth were the mesopelagic crustaceans (Childress 1975) and fishes (Torres et al. 1979, Figure 2.27) off the coast of California. In both cases, the difference in metabolism between a species living in surface waters and one living at 1000 m greatly exceeded that which would be caused by temperature alone. Depending on the time of year, the difference in temperature between surface waters (about 15 °C in fall) and those at 1000 m (about 4 °C year‐round) would yield an expected change of roughly three‐fold, assuming a conventional Q₁₀ of 2–3. That is, metabolism at depth would be about one‐third of that in surface waters if due only to changes in temperature. Instead the change was about 50‐fold in both crustaceans and fishes! A fish dwelling at 1000 m had a metabolic rate about 2% of that of a surface‐dwelling species. The difference in metabolism between a surface‐ and deep‐dwelling fish (or crustacean) is huge, akin to the difference in metabolism between an active fish and a jellyfish (Seibel and Drazen 2007).

      The fact that both pelagic crustaceans and fishes exhibited profound depth‐related declines in metabolism confirmed that the trend was real and not confined to one taxonomic group. The results in turn opened up a Pandora’s Box of questions. Why the decline occurs and how it is biologically achieved spring to mind as appropriate queries. In addition, one might wonder how widespread among oceanic taxa the decline is and whether it only occurs among pelagic species or whether it is also observed in bottom‐dwelling (benthic) species and species that swim just above the bottom, the benthopelagic species. Enough work has been done to answer many of those questions. It is an instructive journey through the literature to see the questions posed and answered and the explanations for the phenomenon evolve.

Figure 2.28 The relationship between water content and minimum depth of occurrence in a group of midwater fishes. Filled symbols represent species which have well‐developed gas‐filled swimbladders. The regression line of water content as a function of depth is for fishes without well‐developed gas bladders.

      Source: Adapted from Childress and Nygaard (1973), figure 1 (p. 1098). Reproduced with the permission of Elsevier.

The first question, why the decline occurs, has been answered in two different ways over the years. Initially, we thought that declining metabolism was a response to the lower food availability at depth. The less energy required for the tasks of daily metabolism such as swimming, circulation of blood, and maintaining a constant internal environment, the more energy that could be devoted to growing bigger faster. The “energy limitation” hypothesis was very attractive, made more so by the fact that a large fraction of the metabolic decline was achieved through a reduction in metabolizing tissue: pelagic crustaceans and fishes become more watery with depth (Figure 2.28). The higher the water content of an individual, the lower its protein content, and because muscle is largely protein, it follows that deeper‐living species have less muscle. Since muscle commands the lion’s share of the energy produced by daily metabolism in most swimming species, watery, deeper‐living crustaceans and fishes naturally have a much reduced metabolism. Curiously, the reduction in metabolism cannot be explained by an increased water content alone, it is far too great. Not only is there less muscle, the muscle itself has a greatly reduced metabolic demand.

As more data were collected on metabolism in pelagic species from different locations and from different taxonomic groups, two important trends emerged. The first was that in strong swimmers with good vision, notably the crustaceans, fishes, and cephalopods, metabolism declined profoundly with depth in all areas of the world ocean where they were surveyed, most notably the Pacific off California and Hawaii, the Gulf of Mexico, and in the isothermal waters of the Antarctic (Figure 2.29, Seibel and Drazen 2007). The second trend was that weakly swimming pelagic species with poor vision, such as the arrow worms (chaetognaths) and jellyfishes (hydro‐ and scyphomedusae) did not exhibit a significant decline in metabolism with depth. Since food availability is lower for all taxa at mesopelagic depths, the energy‐limitation hypothesis would have predicted a decline in metabolism for chaetognaths and medusae as well as fishes and crustaceans. Since that was not observed, the hypothesis clearly needed modification.

Let us think our way through the problem. First, lowering daily maintenance energy is always a highly desirable strategy. The less energy that you use, the less food you require, and a greater percentage of the food energy that you do acquire can be used for growth. The fact that surface‐dwelling fishes, cephalopods, and crustaceans have a much faster pace of metabolism than deeper‐dwelling relatives, means that something about life at depth allows the deeper‐living representatives to get away with employing what would seem to be a universally desirable strategy. What is the difference between surface and depth likely to wield the most influence on species’ characteristics? The answer, in a word, is light. Metabolic response to the decline in temperature with depth is conventional in pelagic species (Q₁₀ = 2 to 3). The lower temperature at mesopelagic depths only explains a fraction of the decline in rate. Salinity does not change enough to make a difference. However, visual predation is commonplace in the epipelagic zone, and, whether predator or prey, a well‐developed swimming ability is necessary for survival. A highly developed swimming ability is less important at mesopelagic depths, where the lower light levels mean that visual ranges are greatly reduced. As the need for locomotory ability is relaxed so is the need for investment in musculature, resulting in much of the observed decline in metabolism with depth of occurrence. The arguments above form the more modern and widely accepted “visual interactions” hypothesis (Childress and Mickel 1985) for the decline in metabolism with depth.