The Biological Productivity of the Ocean PDF

Vol 3 | Issue 6 | 2012 nature Education The Biological Productivity of the Ocean Daniel M. Sigman 1 & Mathis P. Hain 1,2 © 2012 Nature Education Productivity fuels life in the ocean, drives it...

Vol 3 | Issue 6 | 2012 nature Education The Biological Productivity of the Ocean Daniel M. Sigman 1 & Mathis P. Hain 1,2 © 2012 Nature Education Productivity fuels life in the ocean, drives its chemical cycles, and lowers atmospheric carbon dioxide. Nutrient uptake and export interact with circulation to yield distinct ocean regimes. GPP minus the respiration by all organisms in the eco- system. The value of NEP depends on the boundaries What is Ocean Productivity? defined for the ecosystem. If one considers the sunlit Ocean productivity largely refers to the production surface ocean down to the 1% light level (the “eupho- of organic matter by “phytoplankton,” plants suspend- tic zone”) over the course of an entire year, then NEP ed in the ocean, most of which are single-celled. Phy- is equivalent to the particulate organic carbon sinking toplankton are “photoautotrophs,” harvesting light to into the dark ocean interior plus the dissolved organ- convert inorganic to organic carbon, and they supply ic carbon being circulated out of the euphotic zone. this organic carbon to diverse “heterotrophs,” organ- In this case, NEP is also often referred to as “export isms that obtain their energy solely from the respira- production” (or “new production” (Dugdale & Goering tion of organic matter. Open ocean heterotrophs in- 1967), as discussed below). In contrast, the NEP for clude bacteria as well as more complex single- and the entire ocean, including its shallow sediments, is multi-celled “zooplankton” (floating animals), “nek- roughly equivalent to the slow burial of organic mat- ton” (swimming organisms, including fish and marine ter in the sediments minus the rate of organic matter mammals), and the “benthos” (the seafloor community entering from the continents. of organisms). There are no accumulations of living biomass in the The many nested cycles of carbon associated with marine environment that compare with the forests and ocean productivity are revealed by the following defi- grasslands on land (Sarmiento & Bender 1994). Nev- nitions (Bender et al. 1987) (Figure 1). “Gross primary ertheless, ocean biology is responsible for the stor- production” (GPP) refers to the total rate of organic age of more carbon away from the atmosphere than carbon production by autotrophs, while “respiration” is the terrestrial biosphere (Broecker 1982). This is refers to the energy-yielding oxidation of organic car- achieved by the sinking of organic matter out of the bon back to carbon dioxide. “Net primary production” surface ocean and into the ocean interior before it is (NPP) is GPP minus the autotrophs’ own rate of res- returned to dissolved inorganic carbon and dissolved piration; it is thus the rate at which the full metabo- nutrients by bacterial decomposition. Oceanographers lism of phytoplankton produces biomass. “Secondary often refer to this process as the “biological pump,” as production” (SP) typically refers to the growth rate of it pumps carbon dioxide (CO2) out of the surface ocean heterotrophic biomass. Only a small fraction of the or- and atmosphere and into the voluminous deep ocean ganic matter ingested by heterotrophic organisms is (Volk & Hoffert 1985). used to grow, the majority being respired back to dis- Only a fraction of the organic matter produced in solved inorganic carbon and nutrients that can be re- the surface ocean has the fate of being exported to used by autotrophs. Therefore, SP in the ocean is small the deep ocean. Of the organic matter produced by in comparison to NPP. Fisheries rely on SP; thus they phytoplankton (NPP), most is respired back to dis- depend on both NPP and the efficiency with which or- solved inorganic forms within the surface ocean and ganic matter is transferred up the foodweb (i.e., the thus recycled for use by phytoplankton (Eppley & Pe- SP/NPP ratio). “Net ecosystem production” (NEP) is 1 Department of Geosciences, Guyot Hall, Princeton University, Princeton, New Jersey 08544, USA. 2 now at: School of Ocean and Earth Sciences, University of Southampton, Southampton SO143ZH, UK ©2012 Macmillan Publishers Limited. All rights reserved 1 nature Education Vol 3 | Issue 6 | 2012 Phytoplankton SURFACE OCEAN Zooplankton nutrient uptake + + = GPP + = NPP & Bacteria NEP grazing autotrophic respiration nutrient recycling heterotrophic respiration net nutrient supply by upwelling & mixing = NEP = export of particualte & dissolved organic matter Figure 1. Productivity in the surface ocean, the definitions used to describe it, and its connections to nutrient cycling. The blue cycle for “net ecosystem production” (NEP) (i.e. “new” or “export” production) encompasses the “new” nutri- ent supply from the ocean interior, its uptake by autotrophic phytoplankton growth, packaging into large particles by heterotrophic grazing organisms, and sinking of organic matter out of the surface ocean. The red cycle illustrates the fate of the majority of organic matter produced in the surface ocean, which is to be respired by heterotrophic organisms to meet their energy requirements, thereby releasing the nutrients back into the surface water where they can be taken up by phytoplankton once again to fuel “regenerated production.” The green cycle represents the internal respiration of phytoplankton themselves, that is, their own use of the products of photosynthesis for purposes other than growth. These nested cycles combine to yield (1) “gross primary production” (GPP) representing the gross photosynthesis and (2) “net primary production” (NPP) that represents phytoplankton biomass production that forms the basis of the food web plus a much smaller rate of organic matter export from the surface. While the new nutrient supply and export production are ultimately linked by mass balance, there may be imbalances on small scales of space and time, allowing for brief accumulations of biomass. terson 1979) (Figure 1). Most phytoplankton cells are the seafloor is shallow, and sunlight can sometimes too small to sink individually, so sinking occurs only penetrate all the way through the water column to the once they aggregate into larger particles or are pack- bottom, thus enabling bottom-dwelling (“benthic”) aged into “fecal pellets” by zooplankton. The remains organisms to photosynthesize. Furthermore, sinking of zooplankton are also adequately large to sink. While organic matter isintercepted by the seabed, where it sinking is a relatively rare fate for any given particle in supports thriving benthic faunal communities, in the the surface ocean, biomass and organic matter do not process being recycled back to dissolved nutrients that accumulate in the surface ocean, so export of organic are then immediately available for primary produc- matter by sinking is the ultimate fate for all of the nu- tion. The proximity to land and its nutrient sources, trients that enter into the surface ocean in dissolved the interception of sinking organic matter by the shal- form — with the exceptions that (1) dissolved nutrients low seafloor, and the propensity for coastal upwell- can be returned unused to the interior by the circula- ing all result in highly productive ecosystems. Here, tion in some polar regions (see below), and (2) circu- we mainly address the productivity of the vast open lation also carries dissolved organic matter from the ocean; nevertheless, many of the same concepts, albeit surface ocean into the interior, a significant process in modified form, apply to coastal systems. (Hansell et al. 2009) that we will not address further. As organic matter settles through the ocean interior What Does Ocean Productivity Need? and onto the seafloor, it is nearly entirely decomposed back to dissolved chemicals (Emerson & Hedges 2003, Phytoplankton require a suite of chemicals, and Martin et al. 1987). This high efficiency of decomposi- those with the potential to be scarce in surface wa- tion is due to the fact that the organisms carrying out ters are typically identified as “nutrients.” Calcium is the decomposition rely upon it as their sole source of an example of an element that is rapidly assimilated chemical energy; in most of the open ocean, the het- by some plankton (for production of calcium carbonate erotrophs only leave behind the organic matter that is “hard parts”) but is not typically considered a nutrient too chemically resistant for it to be worth the invest- because of its uniformly high concentration in seawa- ment to decompose. On the whole, only a tiny frac- ter. Dissolved inorganic carbon, which is the feedstock tion (typically much less than 1%) of the organic carbon for organic carbon production by photosynthesis, is from NPP in the euphotic zone survives to be buried in also abundant and so is not typically listed among deep sea sediments. the nutrients. However, its acidic form dissolved CO2 is often at adequately low concentrations to affect the Productivity in coastal ecosystems is often dis- growth of at least some phytoplankton. tinct from that of the open ocean. Along the coasts, 2 ©2012 Macmillan Publishers Limited. All rights reserved Vol 3 | Issue 6 | 2012 nature Education light particulate organic carbon (µmol/kg) 0% 100% 0 10 20 30 40 0m limitation nutrient mixed layer euphotic 100m zone DCM 1% 1% thermocline (slow mixing) light limitation 200m July 2008 at the Bermuda Atlantic Time-series Station, (31.8˚N, 64.3˚W). 300m 0 2 4 6 0 100 200 300 16˚C 26˚C N concentration (µmol/kg) chlorophyll a (ng/kg) temperature Figure 2. Typical conditions in the subtropical ocean, as indicated by data collected at the Bermuda Atlantic Time- series Station in July, 2008. The thermocline (vertical temperature gradient) stratifies the upper water column. During this particular station occupation, the shallow wind-mixed surface layer is not well defined, presumably because of strong insolation and a lack of wind that allowed continuous stratification all the way to the surface. Very little sunlight penetrates deeper than ~100 m. New supply of the major nutrients N and P is limited by the slow mixing across the upper thermocline (showing here only the N nutrient nitrate, NO3-). Within the upper euphotic zone, the slow nutrient supply is completely consumed by phytoplankton in their growth. This growth leads to the accumulation of particulate organic carbon in the surface ocean, some of which is respired by bacteria, zooplankton, and other heterotrophs, and some of which is exported as sinking material. The deep chlorophyll maximum (DCM) occurs at the contact where there is adequate light for photosynthesis and yet significant nutrient supply from below. The DCM should not be strictly interpreted as a depth maximum in phytoplankton biomass, as the phytoplankton at the DCM have a particularly high internal chlorophyll concentration. The data shown here is made available by the Bermuda Institute of Ocean Sciences (http://bats.bios.edu) and the Bermuda Bio Optics Project (http://www.icess.ucsb.edu/bbop/). Broadly important nutrients include nitrogen (N), surface ocean, make Si availability a major factor in phosphorus (P), iron (Fe), and silicon (Si). There ap- the broader ecology and biogeochemistry of surface pear to be relatively uniform requirements for N and waters. P among phytoplankton. In the early 1900s, oceanog- Sunlight is the ultimate energy source — directly rapher Alfred Redfield found that plankton build their or indirectly — for almost all life on Earth, including biomass with C:N:P stoichiometric ratios of ~106:16:1, in the deep ocean. However, light is absorbed and to which we now refer as the Redfield ratios (Redfield scattered such that very little of it penetrates below 1958). As Redfield noted, the dissolved N:P in the deep a depth of ~80 m (as deep as 150 m in the least pro- ocean is close to the 16:1 ratio of plankton biomass, ductive subtropical regions, but as shallow as 10 m in and we will argue below that plankton impose this ratio highly productive and coastal regions) (Figure 2). Thus, on the deep, not vice versa. Iron is found in biomass photosynthesis is largely restricted to the upper light- only in trace amounts, but it is used for diverse es- penetrated skin of the ocean. Moreover, across most of sential purposes in organisms, and it has become clear the ocean’s area, including the tropics, subtropics, and over the last 25 years that iron’s scarcity often limits or the temperate zone, the absorption of sunlight causes affects productivity in the open ocean, especially those surface water to be much warmer than the underlying regions where high-N and -P deep water is brought deep ocean, the latter being filled with water that sank rapidly to the surface (Martin & Fitzwater 1988). Re- from the surface in the high latitudes. Warm water is search is ongoing to understand the role of other trace more buoyant than cold, which causes the upper sun- elements in productivity (Morel et al. 2003). Silicon lit layer to float on the denser deep ocean, with the is a nutrient only for specific plankton taxa-diatoms transition between the two known as the “pycnocline” (autotrophic phytoplankton), silicoflaggellates, and ra- (for “density gradient”) or “thermocline” (the vertical diolaria (heterotrophic zooplankton) — which use it to temperature gradient that drives density stratification make opal hard parts. However, the typical dominance across most of the ocean, Figure 2). Wind or another of diatoms in Si-bearing waters, and the tendency of source of energy is required to drive mixing across the diatom-associated organic matter to sink out of the ©2012 Macmillan Publishers Limited. All rights reserved 3 nature Education Vol 3 | Issue 6 | 2012 pycnocline, and so the transport of water with its dis- plants on land. During much of the twentieth century, solved chemicals between the sunlit surface and the it was thought that cells in the range of ~5 to ~100 mi- dark interior is sluggish. This dual effect of light on crons diameter account for most phytoplankton bio- photosynthesis and seawater buoyancy is critical for mass and productivity. This size range is composed the success of ocean phytoplankton. If the ocean did mostly of eukaryotes, organisms whose cells contain not have a thin buoyant surface layer, mixing would complex membrane-bound structures (“organelles”), carry algae out of the light and thus away from their including the cell’s nucleus and chloroplasts. Well- energy source for most of the time. Instead of nearly studied forms of eukaryotic phytoplankton include the neutrally buoyant single celled algae, larger, positively opal-secreting diatoms, prymnesiophytes (including buoyant photosynthetic organisms (e.g., pelagic sea- the CaCO3-secreting coccolithophorids), and the or- weeds) might dominate the open ocean. This hypothet- ganic wall-forming dinoflagellates. The centrality of ical case aside, although viable phytoplankton cells are these organisms in early oceanographic thought was found (albeit at low concentrations) in deeper waters, due to their accessibility by standard light microscopy. photosynthesis limits active phytoplankton growth to Only with recent technological advances have small- the upper skin of the ocean, while upper ocean density er organisms become readily observable, revolution- stratification prevents them from being mixed down izing our view of the plankton. In particular, the cya- into the dark abyss. Thus, most open ocean biomass, nobacteria, which are prokaryotes (lacking a nucleus including phytoplankton, zooplankton, and nekton, is and most other organelles found in eukaryotes), are found within ~200 m of the ocean surface. now known to be important among the phytoplank- At the same time, the existence of a thin buoyant ton. Initially, the cyanobacteria were identified large- surface layer conspires with other processes to impose ly with colonial forms such as Trichodesmium that nutrient limitation on ocean productivity. The export of play the critical role of “fixing” nitrogen (see below). organic matter to depth depletes the surface ocean of However, major discoveries over the last thirty years nutrients, causing the nutrients to accumulate in deep have revealed the prevalence across the global ocean waters where there is no light available for photosyn- of unicellular cyanobacteria of ~0.5 to ~1.5 microns thesis (Figure 2). Because of the density difference diameter. It is now recognized that two cyanobacte- between surface water and the deep sea across most rial genera — Synechoccocus and Prochlorococcus — of the ocean, ocean circulation can only very slowly dominate phytoplankton numbers and biomass in the reintroduce dissolved nutrients to the euphotic zone. nutrient-poor tropical and subtropical ocean (Water- By driving nutrients out of the sunlit, buoyant surface bury et al. 1979, Chisholm et al. 1988). In addition, waters, ocean productivity effectively limits itself. new methods, both microscopic and genetic, are re- Phytoplankton growth limitation has traditionally vealing a previously unappreciated diversity of smaller been interpreted in the context of Liebig’s Law of the eukaryotes in the open ocean. Minimum, which states that plant growth will be as Mapping ecological and biogeochemical functions great as allowed by the least available resource, the onto the genetic diversity of the phytoplankton is an “limiting nutrient” that sets the productivity of the sys- active area in biological and chemical oceanography. tem (de Baar 1994). While this view is powerful, in- Based on observations as well as theory, the smaller teractions among nutrients and between nutrients and phytoplankton such as the unicellular cyanobacteria light can also control productivity. A simple but im- are thought to dominate regenerated production in portant example of this potential for “co-limitation” many systems, whereas the larger eukaryotes appear comes from polar regions, where oblique solar insola- to play a more important role in new production (i.e., tion combines with deep mixing of surface waters to NEP, Figure 1; see below). yield low light availability. In such environments, high- Heterotrophs er iron supply can increase the efficiency with which Just as large eukaryotes were once thought to domi- phytoplankton capture light energy (Maldonado et al. nate the phytoplankton, it was long believed that mul- 1999, Sunda & Huntsman 1997). More broadly, it has ticellular zooplankton of ≥200 microns dominate het- been argued that phytoplankton should generally seek erotrophy — the small crustaceans known as copepods a state of co-limitation by all the chemicals they re- are the prototypical example. We now know that het- quire, including the many trace metal nutrients (Morel erotrophy is often dominated by single-celled eukary- 2008). otes (“microzooplankton,” of ~1 to ~200 microns) and by bacteria (of ~0.3 to ~1 microns), the latter carrying Who Are the Major Players in Ocean out most of the organic carbon decomposition in the Productivity? ocean. The food source of a given form of zooplankton is Photoautotrophs typically driven by its own size, with microzooplankton In contrast to the terrestrial biosphere, most ma- grazing on the prokaryotes and smaller eukaryotes and rine photosynthesis is conducted by single-celled or- multicellular zooplankton grazing on larger eukary- ganisms, and the more abundant of the multicellular otes, both phytoplankton and microzooplankton. Be- forms are structurally much simpler than the vascular cause of their relative physiological simplicity, micro- 4 ©2012 Macmillan Publishers Limited. All rights reserved Vol 3 | Issue 6 | 2012 nature Education low nutrient supply, efficient recycling high nutrient supply, inefficient recycling organic organic direct sinking matter matter grazing NPP grazing NPP small unicellular large large phyto- micro- phyto- multicellular plankton zooplankton plankton zooplankton (0.5-1.5 µm) (1-100 µm) (5-100 µm) (>200 µm) 10% 90% nutrient 50% 50% regeneration nutrient regeneration bacteria bacteria (