The Whale Pump: Marine Mammals Enhance Primary Productivity in a Coastal Basin - journals.plos.org/plosone/article?id=10.1371/journal.pone.0013255Published: October 11, 2010
AbstractIt is well known that microbes, zooplankton, and fish are important sources of recycled nitrogen in coastal waters, yet marine mammals have largely been ignored or dismissed in this cycle. Using field measurements and population data, we find that marine mammals can enhance primary productivity in their feeding areas by concentrating nitrogen near the surface through the release of flocculent fecal plumes. Whales and seals may be responsible for replenishing 2.3×104 metric tons of N per year in the Gulf of Maine's euphotic zone, more than the input of all rivers combined. This upward “whale pump” played a much larger role before commercial harvest, when marine mammal recycling of nitrogen was likely more than three times atmospheric N input. Even with reduced populations, marine mammals provide an important ecosystem service by sustaining productivity in regions where they occur in high densities.
Introduction
The biological pump mediates the removal of carbon and nitrogen from the euphotic zone through the downward flux of aggregates, feces, and vertical migration of invertebrates and fish. Copepods and other zooplankton produce sinking fecal pellets and contribute to downward transport of dissolved and particulate organic matter by respiring and excreting at depth during migration cycles, thus playing an important role in the export of nutrients (N, P, and Fe) from surface waters. Perhaps because of the prevalence of this flux of zooplankton biomass and detritus, it has often been presumed that the fecal matter of top predators such as marine mammals is also lost rapidly to deep waters and the benthos. Yet predators such as whales, pinnipeds, and seabirds must rise to the surface to breathe, and so may play a different role in nutrient cycling.
There is a growing body of evidence supporting the important role of large vertebrates in many ecosystem processes. Grazing animals in the Serengeti, for example, stimulate net primary productivity and carbon sequestration. Changes in vertebrate density and composition can have local and even global impacts: the decline of Pleistocene megafauna may have impacted methane production and thus atmospheric temperature. Similarly, the removal of sperm whales from the Southern Ocean may have diminished this region's role as a reservoir for carbon.
Several lines of evidence indicate that most of the nitrogen released by marine mammals is expected to be in the shallower portion of their depth range: attachment to the surface for respiration, reduced metabolism at depth, physiological response to hydrostatic pressure, a decrease in glomular filtration rate and urine flow during forced diving studies, and observations of buoyant fecal plumes at the surface. As early as 1983, Kanwisher and Ridgway noted that cetaceans could play an analogous role to upwelling, “lifting nutrients from deep waters” and releasing fecal material “that tends to disperse rather than sink when it is released.” Whale foraging dives are characterized by rapid descents and ascents to reduce transit time to prey aggregations and high metabolic rates in gray seals while motionless at the surface support the idea that marine mammals process food during extended surface intervals following deep-water foraging. Even if defecation occurred randomly, it would on average occur higher in the water column than where these animals feed, since they are unlikely to dive deeper than foraging efforts require.
Thus opposing the contribution of zooplankton, such as copepods, to the downward biological pump, cetaceans feeding deep in the water column effectively create an upward pump, enhancing nutrient availability for primary production in locations where whales gather to feed (Figure 1). Released nitrogenous compounds that can be used by primary producers are likely to remain in the euphotic zone, either as urea (the primary mammalian N-excretory product in urine), or as amino-N and NH4+ as the fecal plume material is consumed and metabolized. Pinnipeds that breed on shore and seaside ledges are also a source of nitrogenous nutrients in coastal waters.
Figure 1. A conceptual model of the whale pump.
In the common concept of the biological pump, zooplankton feed in the euphotic zone and export nutrients via sinking fecal pellets, and vertical migration. Fish typically release nutrients at the same depth at which they feed. Excretion for marine mammals, tethered to the surface for respiration, is expected to be shallower in the water column than where they feed.
We examined the relative importance of the whale pump in the Gulf of Maine, a partially isolated, highly productive basin in the western North Atlantic Ocean where nitrogen is generally considered to be the limiting nutrient for phytoplankton growth. Townsend observed that the advective flux of nitrogen from deep and adjacent waters could not sustain primary production in this basin, noting that the “construction of carbon and nitrogen budgets that consider only fluxes into and out of the Gulf, and not internal recycling, will be in error”.
Results and DiscussionField Measurements
We collected and analyzed 16 fecal plume samples during two whale-tagging cruises on Stellwagen Bank. PON concentrations of the humpback fecal plume samples were elevated by as much as two orders of magnitude above typical mixed-layer concentrations for summer in this area. Concentrations of NH4+ in fecal plumes ranged from 0.4 to 55.5 µmol kg−1. All reference samples collected away from visible fecal plumes had concentrations <0.1 µmol kg−1 (the nominal limit of detection), which is typical for summer surface waters. Hence, nearly all of the samples taken near whale fecal plumes had dramatically elevated NH4+. The results of shipboard incubation time-course experiments are plotted in Figures 2a and 2b. These fecal plume samples contain phytoplankton and microbes capable of utilizing NH4+. Thus any change over time would be the net difference between what was produced by microbial activity associated with the feces (presumably gut flora) and the constituent microbial plankton minus the consumption of NH4+ by plankton and microbes. No samples showed a net loss of NH4+ during these experiments.
Figure 2. Shipboard incubation time-course experiments on Humpback whale samples collected on Stellwagen Bank, Gulf of Maine.
(a) Net NH4+ production vs. fecal PON concentration in time course incubations of material collected in whale fecal plumes. Samples 1 and 2 had the highest initial NH4+ concentrations, yet their rates of NH4+ production ranged from the second lowest to the highest in the entire data set. (b) NH4+ concentration vs. incubation time.
The measured NH4+ production rates in incubated samples were strongly correlated with sample PON concentration (Figure 2a), which implicates fecal particulate material as the source of this nitrogen. The highest observed production rate was equivalent to about 50 times a typical plankton assimilation rate during summer in Massachusetts Bay. Rates of increase in NH4+ show no relationship to initial NH4+ concentrations (Figure 2b), suggesting that the source is the fecal particulate material rather than another dissolved compound (amino-N or urea) that was co-released with NH4+.
Ecosystem EffectsWe propose that marine mammals play an important role in the delivery of recycled nitrogen to surface waters (Table 1). Over the course of a year, marine mammals release approximately 2.3×104 metric tons (1.7×109 mol N) per year to the surface of the Gulf of Maine, more than all rivers combined and approximately the same as current coastal point sources (Figure 3a, Table 2,). Although atmospheric deposition delivers more nitrogen to the Gulf than rivers or marine mammals, it is important to note that the atmospheric source is currently much higher than the estimated preindustrial levels (Figure 3b).
Figure 3. The flux of nitrogen in the Gulf of Maine (a) at present and (b) before commercial hunting.
Point-source pollution, industrial emissions of nitrogen, and allochthonous sources from Townsend [18]. The range of historical estimates are adapted from Lotze. Sources that are not expected to be influenced by anthropogenic change, such as offshore transport from Scotian Shelf water, are not included in this graph.
Table 1. Effect of common and historically important marine mammals on the nitrogen cycle in the Gulf of Maine ecosystem.
Table 2. Contemporary nitrogen flux in the Gulf of Maine.
The release of nutrients at the ocean surface is a pattern common to many air-breathing vertebrates, however, in the Gulf of Maine, and presumably in many other systems, it is dominated by whales, especially baleen whales. Currently cetaceans deliver approximately 77% of the nutrients released to the gulf by mammals and birds (Table 2); their biomass in the North Pacific and Southern Oceans indicate that they also play a dominant role in these systems. For some marine ecosystems it may be appropriate to expand this term beyond one that emphasizes whales to acknowledge greater importance of pinnipeds or seabirds. In the gulf, the whale pump will be most active in spring and summer, when feeding whales are present and when nitrate levels are low (Figure 4). Concentrations are ∼8 µmol kg−1 in winter but approach undetectable levels in summer. Kenney et al. have estimated that 30% of the annual prey consumed by cetaceans in the Gulf of Maine occurs in spring and 48% in summer. Surface excretion may extend seasonal plankton productivity during these seasons, after a thermocline has formed. The effects of the pump are also expected to be much greater in highly productive areas such as Stellwagen and Georges Banks and the Bay of Fundy, where diving and surfacing transcends warm-season stratification and can markedly increase surface nitrogen levels.
Figure 4. The role of cetaceans in the nitrogen cycle by season.
Seasonal estimates based on the percentage of total consumption in the Gulf of Maine
The whale pump provides a positive plankton nutrition feedback. On Stellwagen Bank, humpback whales bottom feed on sand lance (Ammodytes spp), especially at night when these forage fish burrow into the sandy substrate. In the Grand Manan Basin, right whales feed beneath the thermocline, on concentrated bands of diapausing copepods, in direct proportion to the abundance and quality of food available. The density of copepods in this layer is orders of magnitude greater than average estimates of water-column prey density. The average dive depth (113–130 m) for right whales is strongly correlated with peak prey abundance (fifth copepodites of Calanus finmarchicus) and the thermocline. Fin whale foraging dives often exceed 100 m to locate dense concentrations of euphausiids.
Not all feeding occurs along or below the pycnocline. Right whales surface feed on copepods in Cape Cod Bay and the Great South Channel in the spring. On Stellwagen, humpbacks tend to surface feed during daylight hours, when their prey is most abundant in the upper portion of the water column. Several species have diel patterns in foraging behavior: sei whales feed on aggregations of C. finmarchicus when they migrate to the surface at night, reducing transit time for the whales and maximizing foraging efficiency. Although the upward movement of nutrients is essential to our conception of the whale pump, the feeding of marine mammals at the surface, especially on prey that migrate across the pycnocline themselves, and the subsequent excretion of nutrients at the surface are important parts of the overall pattern of the pump.
Because of their large size and the high energetic cost of foraging, baleen whales require dense patches of food. Production of phytoplankton stocks that support copepods, euphasiids, and fish consumed by whales will benefit most immediately from the release of nitrogenous excreta in nutrient-limited waters during stratified summer conditions. The whale pump could also reinforce the aggregative behavior and cooperative foraging of some cetaceans. The predictability of finding food in regions of high productivity is critical to individual survival and reproductive success: many species return to the same locations year after year, using the same feeding grounds across generations. Another possible concentration-enhancing mechanism of the whale pump is the attraction of zooplankton to fecal material. The initial observation that led Hamner and Hamner to study the use of scent trails by zooplankton was an aggregation of copepods on the regurgitated meal of a seasick dive-boat tender. At least one of the fecal plumes we collected—suspended just below the surface, about the size of our inflatable sampling boat, and the color of oversteeped green tea—had high numbers of copepods. Consumption of the fine particulate fraction in the fecal plume by zooplankton would provide further nutrition for the lower trophic levels that nourish these mammals.
Any attempt to study the role of marine mammals in coastal ecosystems must consider that many species now occur only in remnant populations, drastically reduced by commercial exploitation, incidental mortality, and habitat destruction (Figure 3b). Three species of mammals (sea mink, Atlantic walrus, and possibly Atlantic gray whale) are now extinct or absent in the Gulf of Maine, along with several marine birds, including the great auk. In the Bay of Fundy, humans have reduced the biomass of the upper trophic level of vertebrates by at least an order of magnitude. One unanticipated consequence of this depletion of deep-diving mammals is a likely decline in the carrying capacity for higher trophic levels in coastal ecosystems.
Looking beyond the Gulf of Maine, it is important to consider the roles of present and past stocks of large air-breathing predators in the nutrient cycle of marine ecosystems. In the North Pacific, whale populations consume approximately 26% of the average daily net primary productivity; pre-exploitation populations may have required more than twice this sum. Might primary productivity have been higher in the past as a result of a stronger whale pump? One recent study provides evidence that phytoplankton abundance has declined in 8 of 10 oceanic regions over the past century, and the authors suggest that this can be explained by ocean warming over this period. Yet declines in both the Arctic and Southern Ocean regions, areas with especially high harvests of whale and seal populations over the past century, are in excess of the mean global rate. Full recovery from one serious anthropogenic impact on marine ecosystems, namely the dramatic depletion of whale populations, can help to counter the impacts of another now underway—the decline in nutrients for phytoplankton growth caused by ocean warming. The whale pump may have even played a role in helping to support a greater number of apex consumers. In the Southern Hemisphere, Willis has noted that a decrease in krill abundance followed the near elimination of large whales. He hypothesized that one factor in this counterintuitive decline is a shift in krill behavior. Another factor could be the diminished whale pump, which would have affected productivity by reducing the recycling of nutrients to near-surface waters: Smetacek and Nicol et al. have shown that whales recycle iron in surface waters of the Southern Ocean. The fertilization events of the whale pump can apply to nitrogen, iron, or other limiting nutrients.
These findings have important implications for the management of ocean resources. As marine mammal populations recover, it has been suggested that whales and other predators should be culled to limit competition with human fishing efforts, an idea that has been championed to challenge international restrictions on whaling. Yet no data have been forthcoming to support the logic of this assertion. Furthermore, recent studies suggest that marine mammals have a negligible effect on fisheries in the North Atlantic; simulated reductions in large whale abundance in the Caribbean did not produce any appreciable increase in biomass of commercially important fish species. On the contrary, marine mammals provide important ecosystem services. On a global scale, they can influence climate, through fertilization events and the export of carbon from surface waters to the deep sea through sinking whale carcasses. In coastal areas, whales retain nutrients locally, increasing ecosystem productivity and perhaps raising the carrying capacity for other marine consumers, including commercial fish species. An unintended effect of bounty programs and culls could be reduced availability of nitrogen in the euphotic zone and decreased overall productivity.
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