Giant Larvacean Houses: Rapid Carbon Transport to the Deep Sea Floor

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Science  10 Jun 2005:
Vol. 308, Issue 5728, pp. 1609-1611
DOI: 10.1126/science.1109104


An unresolved issue in ocean science is the discrepancy between the food requirements of the animals living on the deep sea floor and their food supply, as measured by sediment traps. A 10-year time-series study of the water column off Monterey Bay, California, revealed that the discarded mucus feeding structures of giant larvaceans carry a substantial portion of the upper ocean's productivity to the deep seabed. These abundant, rapidly sinking, carbon-rich vectors are not detected by conventional sampling methods and thus have not been included in calculations of vertical nutrient flux or in oceanic carbon budgets.

Most deep benthic communities are supplied with food by a process described more than a century ago as a “rain of detritus” (1). The vertical flux of organic carbon in small particles, fecal pellets, and aggregates of marine snow is typically measured by sediment traps (2). Most of the particles that reach the deep sea floor are less than 5 mm in size, sink slowly, and have organic carbon levels that are reduced by microbial mineralization during their descent, which may last for months (3, 4). Pulses of small particle flux are coupled to surface productivity (57). In studies of the relationship between organic carbon flux and the nutritional requirements of the deep benthic fauna, there is a discrepancy between the amount of food used by these animals and what can be accounted for by sediment traps on the supply side (810). This gap may be linked to declines in productivity that have accompanied the recent warming of the upper ocean (9, 1113). A number of secondary sources have been suggested that might make up the difference between supply and demand, including carrion falls, pulses of phytodetritus, and lateral transport from continental shelves (9, 1416). All of these probably contribute to the deep benthic food supply, but none have been shown to occur in sufficient quantity or with the consistency necessary to compensate for the disparity.

Here we discuss a class of particles consisting of the large, discarded feeding structures of giant mesopelagic larvaceans (appendicularians). These planktonic tunicates feed on suspended particles by secreting intricate filtration structures made of mucopolysaccharides (Fig. 1A), through which they pump water by beating their tails (17). An active filter structure is called a “house” because the animal lives inside it. Typically, each house has two nested filters: a coarse outer mesh and a fine-mesh inner structure. Giant larvaceans attain lengths up to 60 mm, and their houses are frequently greater than a meter in diameter (17, 18).

Fig. 1.

In situ video frame grabs of steps in the progression from an actively filtering giant larvacean house to a descending sinker. (A) An active house occupied by Bathochordaeus; the coarse mesh outer filter surrounds a fine mesh inner filter, to which the tadpole-shaped animal is attached. (B) An abandoned and collapsed house, with most of the outer filter condensed into ropy strands and a small portion domed over the inner filter. (C) As the sinker rapidly descends, the mass becomes more compacted, and the inner filter is usually the last part to collapse. Scale bars: (A) and (B), 10 cm; (C), 1 cm.

The first giant larvacean identified, Bathochordaeus charon, was discovered in 1898, but their feeding structures were unknown until the 1960s, when they were observed during submersible dives (18). Subsequently, giant larvacean houses have been reported by observers using undersea vehicles in the eastern and western Pacific and in the Atlantic (17, 19, 20). These large houses are very fragile and do not survive capture by plankton nets. As a consequence, their potential contribution to vertical carbon flux was not recognized until they were observed in situ (21).

Larvacean houses are disposable, and when one becomes clogged with particles, the animal simply discards it and makes another. The structures collapse when water is no longer pumped through them (Fig. 1B). Once abandoned, they sink rapidly to the sea floor at a rate of ∼800 m day–1 (17). At this rate, there is little time for mineralization by microbes. Discarded houses have not been accounted for by conventional methods for sampling sinking detritus (22), and thus their contribution to nutrient flux has not been factored into oceanic carbon budgets (23).

We used remotely operated vehicles (ROVs) to measure the abundance of both occupied and discarded giant larvacean houses (called “sinkers”) and to collect them for chemical analyses. Abundance was measured by quantitative video transects at 100-m depth intervals, down to 1000 m, on about a monthly basis from 1994 through 2003. By calibrating a camera to record a measured area and then measuring the distance traveled during each transect, we were able to examine a known volume of water at each depth (24).

Samples for chemical analysis were collected with specialized samplers by skilled pilots, who carefully positioned the open containers around the delicate sinkers, then gently sealed them inside. Because the sinkers are so very easily fragmented and dispersed, only about 1 in 4 of our collection attempts was successful, and it is easy to see how sediment traps have missed them (25). As the sinkers descend, hydrodynamic forces shape them into increasingly compact forms (Fig. 1C); nevertheless, they remain easily disrupted by mechanical contact.

We surveyed the water column at three sites along the axis of the Monterey Canyon, off the California coast. These direct observations revealed a distinct class of large sinking aggregates, clearly derived from giant larvacean houses. The midwater fauna off Monterey Bay contains at least three giant larvacean species, each with a characteristic depth range and alarge(>30 cm in diameter), distinctive house (2628). The abundance of occupied houses and sinkers varied seasonally and interannually, but both were present year-round (Fig. 2). Estimates of the house-production rate of Bathochordaeus range from one per day (16) to one per month (17). On the basis of our counts of occupied houses, sinkers, and their sinking rate, we calculate that Bathochordaeus produces a new house every day (24) (Fig. 3). Sinkers are commonly observed during dives along the floor of the Canyon, with densities as high as 1 sinker per m2 (17). Over the 10-year span of this study, the average flux of sinkers to the sea floor was 3.9 m–2 day–1. We measured the particulate organic carbon (POC) and dissolved organic carbon content of 105 sinker samples, collected over a 2-year period at depths from 200 m to 2979 m (24). The average of total organic carbon was 5.4 mg, and the average C:N ratio was 6.09.

Fig. 2.

Carbon flux (gray area) to the deep sea floor and the abundance of active (dotted blue line) and discarded (dotted red line) giant larvacean houses. Data collected in a 10-year ROV-based time series in Monterey Bay, California, show a consistent supply of carbon over summer (s), fall (f), and winter (w) seasons. Integrated primary productivity values (green line) and temperatures (at the surface, solid red line; at 200-m depth, solid blue line) were taken at a permanent mooring adjacent to the transect site (32). A negative exponential (second-degree polynomial function) was used to smooth the temperature and integrated carbon data.

Fig. 3.

Comparative plot of active houses of giant larvaceans (blue line) and discarded sinkers (red line) versus depth, in square meters of area swept. The data are derived from a 10-year time series of quantitative video transects at depth intervals between 100 and 1000 m (n = 679 transects). With an average sinking rate of 800 m day–1, the difference between the integrated areas beneath the curves indicates that these animals produce a new house each day (24).

When we calculate nutrient flux by multiplying the average organic carbon content of a sinker by the number reaching the bottom each year, we get a rate of 7.6 g of C m–2 year–1 (Fig. 2). Data from sediment traps deployed in the same region as our dive sites have shown annual carbon flux rates from 14.4 to 24.0 g of C m–2 year–1 at depths around 500 m and from 7.2 to 14.4 g of C m–2 year–1 at sea-floor depths (16, 2931). Our calculations of sinker carbon flux are conservative because (i) we undercounted the number of deep sinkers, which are more compact, sink faster, and thus are less likely to be seen; (ii) our sampling was biased toward smaller specimens, because large sinkers did not fit into our samplers; and (iii) we did not count sinkers that had fragmented naturally. Although the measured flux of sinker carbon was variable, the changes did not appear to be closely linked to gross primary production, temperature, or season (32) (Fig. 2).

The discarded houses of giant larvaceans thus compose a distinct class of sinking particles that provide a substantial portion of the vertical carbon flux in the deep water column. This is the case off Monterey Bay and probably elsewhere as well. The balance of POC supply and demand measured by Smith and Kaufmann (9) at a deep benthic station off central California ranged from occasional surpluses to extended discrepancies of 8 mg of C m–2 day–1 or more over 7 years. In Monterey Canyon, the daily average of carbon transport by sinking larvacean houses was more than enough to close this gap. Present-day models of carbon flux through the deep water column predict that only ∼10% of the POC that sinks below 100 m reaches depths beyond 1000 m (33). Our results reveal a pathway through this region that carries substantially more carbon than has been measured by conventional methods. Carbon that reaches the deep sea floor is effectively removed from the atmosphere for geological time scales (33).

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