PerspectiveOcean Science

Animal Function at the Heart (and Gut) of Oceanography

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Science  16 Jan 2009:
Vol. 323, Issue 5912, pp. 343-344
DOI: 10.1126/science.1161618

Far more biomass is contained in marine primary producers than in marine animals at higher levels of the food chain. This relation suggests that animals—particularly secondary consumers such as fishes—must play a negligible role in elemental cycling in the world's oceans (1). However, given that the midwater ecosystem is the largest on Earth, with over 99.5% of the habitable space (2), the activity and metabolism of oceanic animals across great depth ranges, especially in productive regions, should perhaps not be discounted (3, 4). Unfortunately, marine animal biomass, distribution, and function are not sufficiently well known to fully reconcile these opposing views (5). On page 359 of this issue, Wilson et al. (6) elucidate a physiological pathway, common to all marine bony fishes, that seems to contribute substantially to the marine inorganic carbon cycle.

The first clue to a possible role of fish in the marine inorganic carbon cycle came from studies of toadfish, Opsanus beta. In 1991, while investigating the fate of urea-derived carbon, Walsh et al. observed pellets in the toadfish's gut (7), which were later found to be a metastable form of calcite that contains large amounts of magnesium. The source of these “gut rocks” was not immediately obvious, but Walsh et al. reasoned that if common to all fish, they might contribute to the inorganic carbon cycle.

More than a decade of detailed physiology has revealed how and why gut rocks form. As far as is known, all bony fishes regulate their internal osmolarity at a level considerably lower than that of seawater and, in seawater, must drink to remain hydrated. However, absorption of the imbibed fluid by the intestine is osmotically limited by the concentrated ions in seawater. Active acid-base regulation facilitates precipitation of the divalent ions as gut rocks and promotes fluid absorption. This appears to be a universal phenomenon critical to the survival of all marine-adapted bony fishes.

For most of the past century, substantial dissolution of calcium carbonate (CaCO3) was believed to occur only in the deep waters that are undersaturated with respect to the various phases of calcium carbonate. However, more recent observations of water column alkalinity reveal that substantial dissolution of calcium carbonate must be occurring at depths well above this “chemical lysocline” (8). The most likely explanation is dissolution of more soluble forms of calcium carbonate, such as the aragonitic shells of pteropod mollusks. More studies on CaCO3 are needed, particularly in remote regions like the Southern Ocean (9), but current estimates of such sources fail to explain all of the mysterious alkalinity. One possible source is the high-magnesium calcite from which gut rocks are formed; its lysocline is shallower than that for other forms of carbonate, and gut rocks would therefore dissolve at shallower depths. However, few oceanographers took note of Walsh's gut rock hypothesis.

An unexpected role.

Fishes at the top of the trophic pyramid are traditionally considered unimportant for biogeochemical cycles because of the loss of energy as one moves from low to higher levels in the food chain. This stylistic pyramid shows how marine fish, as first discovered in the toadfish Opsanus beta (top), produce precipitated carbonates (“gut rocks”) within their intestines (middle) (6) and make a substantial contribution to the global calcium carbonate cycle (bottom) (estimated CaCO3 concentrations for the world oceans).

CREDITS: (TOP) USGS; (MIDDLE) FROM (6); (BOTTOM) NASA AQUA MODIS SATELLITE IMAGE

Wilson et al. have now modeled the size, composition, and abundance of marine fish across the global ocean using two different approaches. Each relies on satellite-derived estimates of global primary productivity from phytoplankton and the conversion of organic matter from one trophic level or link in the food chain to the next (10) (see the figure). It is thus imperative, particularly in this era of climate change, that satellite assets be maintained and expanded via consistent national investment to produce quality imagery (11) that can be used not only to assess traditional phytoplankton concentrations but also to model top-down linkages in the food chain (6, 12, 13). Because of the immensity of the oceans, small variations in model assumptions can swell into vastly different global results. Nevertheless, when coupled with global models and estimates of sea surface temperature, the present analysis predicts substantial fish carbonate production across the world ocean—enough to explain at least one-quarter of the increased alkalinity, or 3 to 15% of total oceanic carbonate production.

Comparative physiology is a thriving field, but is rarely applied to oceanographic problems. Wilson et al. (6) show convincingly that animals, even in the upper trophic levels, can affect elemental cycles via their physiological manipulations. Previous studies have recognized several mechanisms by which animals may contribute to such cycles. For example, many oceanic animals undergo diel vertical migrations from their shallow feeding grounds to depths of several hundred meters, where they continue to excrete respiratory carbon dioxide, effectively pumping carbon out of the atmosphere to the deep sea (3). Metabolic suppression and anaerobic metabolism, used by some migrators during daytime forays into expansive oxygen minimum zones, may reduce the efficiency of this biological carbon pump in some regions (14). The efficiency of carbon pumping is similarly reduced in the Southern Ocean, where air-breathing mammals and birds are a key component of the food chain. They respire massive amounts of photosynthetically derived carbon back into the atmosphere (13). In contrast, larvaceans increase carbon flux by concentrating particles in their mucus feeding webs that then sink rapidly to depth (15). All these processes depend on the demand for energy, which varies between species by up to three orders of magnitude [see supporting online material (6)].

Despite their potential importance, these and similar phenomena remain poorly constrained for most oceanic taxa. It is thus difficult to estimate or predict the role of animal function in biogeochemical cycles. The relevant processes must be recognized and quantified, their rates scaled up, and put in the context of global elemental budgets. Wilson et al.'s important contribution to our knowledge of the inorganic carbon cycle will hopefully infuse a new appreciation for the role of higher trophic levels in ocean dynamics. Clearly, the field is moving beyond the dismissive viewpoint described by Horne, in which animals were merely a source of “heterogeneity in the sea” [(16), p. 239]. As he noted, “Our element of seawater may well contain an important second phase we have not mentioned—a fish” [(16), p. 3].

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