Читать книгу Life in the Open Ocean - Joseph J. Torres - Страница 60

By now you may be growing to appreciate the profound changes in the physical environment of the open ocean in the horizontal and vertical planes and their effects on the physiology of open‐ocean fauna. Deeper‐living species 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.

Figure 2.29 Metabolic rates of diverse marine species as a function of minimum habitat depth. (a) Pelagic groups with image‐forming eyes, including fish (closed circles), cephalopods (plus signs) and crustaceans (open squares); (b) pelagic taxa lacking image‐forming eyes, including chaetognaths (open circles) and medusae (closed circles).

Source: Seibel and Drazen (2007), figure 1(a) and (b) (p. 3). Republished with the permission of The Royal Society (U.K.), from The Rate of Metabolism in Marine Animals: environmental constraints, ecological demands and energetic opportunities, B.A. Seibel and J. C. Drazen, Philosophical Transactions, Biological Sciences, volume 362, issue 1487, © 2007; permission conveyed through Copyright Clearance Center, Inc.

We have already noted that part of the decline in metabolic rate with depth is the result of a more watery structure in deeper‐living species, including a lower protein and, by implication, lower muscle content. Further studies revealed that there are also changes in the muscle itself. Activity of the important intermediary metabolic enzymes lactate dehydrogenase and citrate synthase declines with the depth of occurrence in both California and Antarctic pelagic fishes. In fact, the slopes are very similar to that observed in the decline of oxygen consumption rate with depth (Figure 2.30) (Childress and Somero 1979; Torres et al. 1979; Torres and Somero 1988; Childress and Thuesen 1995; Seibel and Drazen 2007). Thus, not only is there less muscle in deeper‐living species but the muscle that is present is less metabolically active.

Figure 2.30 Activities of the respiratory enzymes citrate synthase (aerobic; closed symbols) and lactate dehydrogenase (anaerobic; open symbols) in marine animals as a function of minimum depth of occurrence. (a) Pelagic fish; (b) pelagic cephalopods.

Source: Seibel and Drazen (2007), figure 4 (p. 7). Republished with the permission of The Royal Society (U.K.), from The Rate of Metabolism in Marine Animals: environmental constraints, ecological demands and energetic opportunities, B.A. Seibel and J. C. Drazen, Philosophical Transactions, Biological Sciences, volume 362, issue 1487, © 2007; permission conveyed through Copyright Clearance Center, Inc.

Our last question on the decline in metabolism with depth is whether it is confined to pelagic species or whether it can be observed also in benthic and benthopelagic species. Keep in mind that the benthos and the pelagial are fundamentally quite different in their potential food availability. The pelagic realm does not retain the organic matter raining from the sunlit waters above, it’s “just passing through.” Large near‐neutrally‐buoyant particles may move through slowly but move through they do. In contrast, the benthos is the final resting place for the organic rain from the surface, however diminutive that rain may be. Even in non‐productive waters, the benthos is a predictably richer environment than the deep pelagic realm. Also, due to episodic events like food‐falls (those dead whales have to go somewhere), the richness of the environment can vary considerably in the horizontal plane. Thus for mobile species like crabs, shrimps, and fishes, the ability to move well can be very beneficial. Because benthic species like crabs have their weight supported by the sea floor, they do not need to worry about buoyancy. Similarly, though buoyancy is a concern for benthopelagic fishes, changes in their vertical profile are minimal and allow the use of a swim bladder. The advantage of being able to move quickly to a food‐fall might make it advantageous to retain a robust musculature.

Does a change in metabolism with depth occur in all open‐ocean taxa? Data show that assumption to be both right and wrong, depending upon the taxa of interest. Benthic Crustacea show no change in metabolism with depth of occurrence outside of that predicted by the declining temperature with depth (Childress et al. 1990), a trend very different from that of their pelagic counterparts. Fishes are another matter. Benthic and benthopelagic fishes both show marked declines in metabolism with depth of occurrence (Smith and Brown 1983; Drazen and Seibel 2007), though the slopes for the trend are slightly less than those observed in pelagic species. As in pelagic fishes, the declines in oxygen consumption rate with depth are mirrored by similar declines in enzyme activities (Drazen and Seibel 2007).

The benthic and benthopelagic fishes that have been studied are quite a bit larger than the pelagic species, generally at least 10 times larger and sometimes as much as 100–1000 times (Drazen and Seibel 2007). As adults at least, they are far more likely to be predators than to be prey. Reduced light levels at depths >500 m restrict visual ranges just as profoundly on the bottom as they do in the midwater, so active searching for prey is likely to be a high‐cost/low‐benefit activity even though hunting is essentially restricted to the horizontal plane. It is thus beneficial for bottom‐oriented fishes to cut daily maintenance costs just as the pelagic species do. The tradeoff is a slower journey to the occasional food‐fall, but obviously evolution has assured that it is fast enough.