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The Metabolism of Aquatic Ecosystems: History, Applications, and Future Challenges

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The Metabolism of Aquatic Ecosystems: History, Applications, and Future Challenges Aquat Sci (2012) 74:15–29 DOI 10.1007/s00027-011-0199-2 Aquatic Sciences OVERVIEW The metabolism of aquatic ecosystems: history, applications, and future challenges Peter A. Staehr • Jeremy M. Testa • W. Michael Kemp • Jon J. Cole • Kaj Sand-Jensen • Stephen V. Smith Received: 18 June 2010 / Accepted: 15 March 2011 / Published online: 30 March 2011 Ó Springer Basel AG 2011 Abstract Measurements of the production and con- and managing aquatic systems. We identify four broad sumption of organic material have been a focus of aquatic research objectives that have motivated ecosystem metab- science for more than 80 years. Over the last century, a olism studies: (1) quantifying magnitude and variability of variety of approaches have been developed and employed metabolic rates for cross-system comparison, (2) estimating for measuring rates of gross primary production (Pg), res- organic matter transfer between adjacent systems or sub- piration (R), and net ecosystem production (Pn = Pg - R) systems, (3) measuring ecosystem-scale responses to within aquatic ecosystems. Here, we reconsider the range of perturbation, both natural and anthropogenic, and (4) approaches and applications for ecosystem metabolism quantifying and calibrating models of biogeochemical measurements, and suggest ways by which such studies can processes and trophic networks. The magnitudes of whole- continue to contribute to aquatic ecology. This paper system gross primary production, respiration and net eco- reviews past and contemporary studies of aquatic ecosys- system production rates vary among aquatic environments tem-level metabolism to identify their role in understanding and are partly constrained by the chosen methodology. We argue that measurements of ecosystem metabolism should Electronic supplementary material The online version of this be a vital component of routine monitoring at larger scales article (doi:10.1007/s00027-011-0199-2) contains supplementary in the aquatic environment using existing flexible, precise, material, which is available to authorized users. and durable sensor technologies. Current and future aquatic ecosystem studies will benefit from application of new P. A. Staehr (&) Department of Marine Ecology, National Environmental methods for metabolism measurements, which facilitate Research Institute, Aarhus University, Frederiksborgvej 399, integration of process measurements and calibration of PO Box 4000, Roskilde, Denmark models for addressing fundamental questions involving e-mail: [email protected] ecosystem-scale processes. J. M. Testa Á W. M. Kemp Horn Point Laboratory, Center for Environmental Science, Keywords Aquatic ecosystems Á Metabolism Á University of Maryland, PO Box 775, Cambridge, Methods Á History Á Applications Á Future MD 21613, USA J. J. Cole Cary Institute of Ecosystem Studies, Box AB, Millbrook, Introduction NY 12545-0129, USA The dynamic nature of food webs and biogeochemical K. Sand-Jensen Freshwater Biological Laboratory, University of Copenhagen, cycles in aquatic ecosystems is tied to metabolic processes Helsingørsgade 51, 3400 Hillerød, Denmark that involve the formation and/or utilization of organic matter (O’Neill 1986; De Angelis 1992). The combined S. V. Smith anabolism and catabolism of all organisms within an eco- Departamento de Geologı´a, Centro de Investigacio´n Cientifica y de Educacio´n Superior de Ensenada, Ensenada, system can be summed to quantify the metabolism of that Baja California, Mexico ecosystem. This metabolism represents an integrated 123 16 P. A. Staehr et al. measure of a system in terms of its overall rates of pro- representative and sufficiently large to provide a broad duction and consumption of organic matter (Odum 1971). overview of methods and applications of aquatic Efforts to quantify metabolism initially developed in par- metabolism. allel to ecosystem science, and as a result, have been highly influential in the development of aquatic ecology (Juday 1940; Lindeman 1942; Dineen 1953; Odum and Odum Essential terms used in ecosystem metabolism studies 1955; Woodwell and Whittaker 1968). Such measurements should continue to be an essential component of aquatic Many terms have been widely used in the literature to ecology in understanding large and complex changes to the describe rates of ecosystem-level primary production and biosphere. respiration. Gross primary production (Pg) is defined as the Aquatic ecosystem metabolism has been determined total autotrophic conversion of inorganic carbon to organic with an increasingly diverse collection of methods, all of forms, independent of its fate. Ecosystem respiration (R) is which have their limitations and strengths (Gazeau et al. the total oxidation of organic C to inorganic C by both 2005a; Kemp and Testa 2011). The methods vary widely in heterotrophic and autotrophic organisms, with alternative precision and temporal/spatial scale, and differ in their notations including Re, ecosystem R, ER, or where a utility to measure gross or net processes. While no single method measures only a subset of the ecosystem compo- method is perfect, the diversity and flexibility of the vari- nents, community R or CR. Net ecosystem production (Pn) ous methods allow for their application in studies of is the difference between Pg and R, and reflects the balance streams, rivers, lakes, estuaries, and the open ocean. Given between all anabolic and catabolic processes. From a con- the long research history of these measurements, it is useful ceptual viewpoint it is useful to partition Re into the to reconsider the range of successful applications, and their respiration of the autotrophs themselves (Ra) and that of the role in aquatic ecological research. heterotrophic organisms (Rh) (Lovett et al. 2006; Dodds and Although much has been learned during this long his- Cole 2007). Methodological constraints have, however, tory, many questions remain regarding the influences of limited the ability to distinguish autotrophic from hetero- widespread anthropogenic perturbations on aquatic eco- trophic respiration (del Giorgio and Williams 2005). systems, especially in poorly studied regions (Dodds and Assuming that Ra can be determined, it is possible to Cole 2007; Williamson et al. 2008). We describe here the quantify the portion of primary production available for rich and diverse contributions of ecosystem metabolism consumption, referred to as net primary production studies to the field of aquatic science, with an emphasis on (NPP = Pg - Ra, Fig. 1, Woodwell and Whittaker 1968; methodological development and lessons learned from past Lovett et al. 2006; Cole et al. 2006). New terms for eco- research. We also identify future challenges for ecosystem system metabolism have also appeared with the metabolic studies including: (1) development of robust and development of novel techniques, including gross oxygen flexible tools to quantify error associated with scaling and production (GOP), which is the anabolic rate derived for the extrapolation, (2) matching methods with appropriate triple oxygen isotope technique (e.g. Luz and Barkan 2000). applications, and (3) understanding the role of climate Usually, different terms have been used for describing change in aquatic metabolic balances. aquatic versus terrestrial ecosystem metabolism (Lovett et al. 2006; Chapin et al. 2006). In aquatic science, GOP and net community production (NCP) are comparable to Pg Literature survey and Pn, respectively. GOP is used when O2 is measured instead of carbon (Luz and Barkan 2000), and NCP is often The quantitative basis for this paper is a thorough review of used when just the pelagic aquatic community is being text books and 350 published papers about aquatic eco- measured (e.g. Sweeney et al. 2000). Although Pn has been system metabolism during the past century. Peer reviewed measured from the summation of container incubations or journal articles were initially collected in ISI web of water column changes in dissolved inorganic carbon or O2, knowledge using a search profile with ‘‘metabolism’’, in most cases it can also be computed from import–export ‘‘production’’ and, ‘‘respiration’’ in combination with lakes, budgets (e.g. Kemp et al. 1997; Dillon and Molot 1997). rivers, streams, estuaries, and oceans. Then, a backward Thus, Pn becomes equivalent to the carbon export (Cexport) search strategy was applied providing articles citing older minus carbon import (Cimport) plus the change in storage of central articles on aquatic ecosystem metabolism. Finally, organic material (delCorg or just DCstorage, Fig. 1): articles were found via citations in textbook chapters on Pn ¼ DCstorage þ Cexport À Cimport: ð1Þ aquatic ecosystem metabolism. Although the list of papers reviewed is not exhaustive, as there have been published When considering long time frames, DCstorage is usually several thousands of articles on this subject, it is equated with the organic C that is buried in soils or 123 Why measure aquatic ecosystem metabolism? 17 Fig. 1 Fates of organic carbon (C) fixed in or imported into an primary production; CO2, carbon dioxide; UV, ultraviolet. Dashed aquatic ecosystem. Total ecosystem respiration (Re) is the sum of lines represent degradation of C, solid lines production and/or transfer autotrophic respiration (Ra) and heterotrophic respiration (Rh). of C. Net autotrophic ecosystems (Pn [ 0) have a net accumulation Accumulation in biomass represents all biomass (plant, animal, or and/or net export organic matter, contrary to net heterotrophic microbial); the arrow is drawn from
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