Discovery of "island mass effect" fueled by nitrogen fixation and its potential impact on biogeochemical cycles in the Pacific Ocean
Takuhei Shiozaki, Atmospheric Ocean Research Institue, The University of Tokyo
Subtropical and tropical oligotrophic oceans have traditionally been recognized as “oceanic deserts”, where nutrient supply (especially nitrogen) is limited due to the strong stratification, and where biological production is generally low. In these oceanic deserts, enhanced primary production and rich fishery resources have been identified around islands where distinctive nutrient supply occurs, a phenomenon referred to as the island mass effect (Doty and Oguri, 1956). The most well-known nutrient supply process is upwelling in an island’s wake, which induces a bloom of chain-forming diatoms (Furuya et al., 1986; Takeda et al., 2007; Hasegawa et al., 2009) (Fig. 1a). This is because diatoms are capable of growing more rapidly than other phytoplankton under light-saturated and nutrient-replete conditions (Furuya et al., 1986). In contrast, our previous basin-scale study in the Pacific Ocean demonstrated that the cyanobacterial genus Trichodesmium, rather than diatoms, increased around islands and conducted active nitrogen fixation (Shiozaki et al., 2010). Since diazotrophs use dinitrogen gas as their nitrogen source, their growth is not limited by nitrogenous nutrients. Meanwhile, Trichodesmium require much more iron for their growth than other phytoplankton due to the necessity of synthesizing the enzyme nitrogenase (Kustka et al., 2002). Therefore, they can thrive around islands where the iron input to the ocean is expected to be high. This anomaly in the phytoplankton community has been considered a local phenomenon. However, our recent study suggests that diazotrophs growing around islands could be delivered horizontally by currents, thereby elevating primary production in more remote areas beyond the island due to a supply of nitrogenous nutrients by nitrogen fixation (Shiozaki et al., 2013).
We conducted trans-Pacific observations from South America to Australia at 17°S (Fig. 2) and examined nitrogen fixation activity and the δ15N of suspended particles (Shiozaki et al., 2014). The latter has proven to be useful for identifying nitrogen sources for the plankton community, and evaluating the spatial extent of nitrogen fixation (Reynolds et al., 2007). We found that in the western subtropical South Pacific, Trichodesmium spp. thrived around islands and performed active nitrogen fixation (Fig. 3a, b), and that their abundance was attributable to the material supplied by land runoff. The Trichodesmium spp. were advected to areas remote from these islands, and as a consequence, the elevated primary production fueled by nitrogen fixation extended over a large area (up to distances of ~3500 km) around the islands (Fig. 1b). This wide expansion of high primary production was characterized by a low δ15N of suspended particles (Fig. 3c) and a large-scale reduction in phosphate concentrations at the surface (Fig. 3d) compared with the subtropical gyre and eastern equatorial upwelling. The occurrence of this vast ecosystem is triggered by terrigenous nutrient supply, suggesting its potential vulnerability to human activity on small islands. More recently, we found that the same phenomenon occurred around islands located along the Kuroshio Current (Shiozaki et al., under revision, PLoS ONE). Nitrogen fixation in the Kuroshio is recognized to be relatively high in the North Pacific, and to influence the nitrogen inventory in the North Pacific (Shiozaki et al., 2010). We demonstrated that the active nitrogen fixation in the Kuroshio is attributable to the island mass effect, i.e. islands situated along the Kuroshio function as manufacturing plants for Trichodesmium, and increased levels of Trichodesmium around the islands are likely to be delivered to the Kuroshio. This leads to the inference that a change in land use on the islands could eventually influence the biogeochemistry in the North Pacific. The impact of the island mass effect on biogeochemical cycles in the open ocean has been ignored. Our study shows that the island mass effect would be a key process to establish ocean provinces.
Fig. 1. a) A diatom bloom in an island’s wake. b) Island mass effect fueled by nitrogen fixation. Trichodesmium spp. (red bars) thrive around islands due to land drainage (white arrows) increasing during the rainy season. The Trichodesmium spp. were advected to areas remote from these islands, and as a consequence, the elevated primary production (yellow circles denote phytoplankton) fueled by nitrogen fixation extended over a large area around the islands.
Fig. 2. Sampling stations in the South Pacific. Background contours represent satellite-derived chlorophyll a during the cruise period.
Fig. 3. Longitudinal surface distribution of (a) abundance of Trichodesmium, spp., (b) nitrogen fixation activities (bulk water and <10 µm), (c) δ15N of suspended particles, and (d) nitrate + nitrite and phosphate.
Doty, M., M. Oguri (1956), The island mass effect, J. Cons. Perm. Int. Explor. Mer., 22, 33-37.
Furuya, K., M. Takahashi, T. Nemoto (1986), Summer phytoplankton community structure and growth in a regional upwelling area off Hachijo Island, Japan, J. Exp. Mar. Biol. Ecol., 96, 43-55.
Hasegawa, D., M.R. Lewis, A. Gangopadhyay (2009), How islands cause phytoplankton to bloom in their wakes, Geophys. Res. Lett., 36, doi:10.1029/2009GL039743.
Kustka, A., S. Sañudo-Wilhelmy, E.J. Carpenter, D.G. Capone, J.A. Raven (2003), A revised estimate of the iron use efficiency of nitrogen fixation, with special reference to the marine cyanobacterium Trichodesmium spp. (Cyanophyta), J. Phycol. 39, 12-25.
Reynolds, S.E., R.L. Mather, G.A. Wolff, R.G. Williams, A. Landolfi, R. Sanders, E.M.S. Woodward (2007), How widespread and important is N2 fixation in the North Atlantic Ocean?, Glob. Biogeochem. Cycles, 21, doi:10.1029/2006GB002886.
Shiozaki, T., K. Furuya, T. Kodama, S. Kitajima, S. Takeda, T. Takemura, J. Kanda (2010), New production of N2 fixation in the western and central Pacific Ocean and its marginal seas, Glob. Biogeochem. Cycles, 24, doi:10.1029/2009GB003620.
Shiozaki, T., T. Kodama, S. Kitajima, M. Sato, K. Furuya (2013), Advective transport of diazotrophs and importance of their nitrogen fixation on new and primary production in the western Pacific warm pool, Limnol. Oceanogr., 58, 49-60.
Shiozaki, T., T. Kodama, K. Furuya (2014), Large-scale impact of the island mass effect through nitrogen fixation in the western South Pacific Ocean, Geophys. Res. Lett., 41, 2907-2913, doi:10.1002/2014GL059835.
Takeda, S., N. Ramaiah, M. Miki, Y. Kondo, Y. Yamaguchi, Y. Arii, F. Gómez, K. Furuya, W. Takahashi (2007), Biological and chemical characteristics of high-chlorophyll, low-temperature water observed near the Sulu Archipelago, Deep-Sea Res. II, 54, 81-102.