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Can Algal Photosynthetic Inorganic Carbon Isotope Fractionation Be Predicted in Lakes Using Existing Models?

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Can Algal Photosynthetic Inorganic Carbon Isotope Fractionation Be Predicted in Lakes Using Existing Models? Aquat. Sci. 68 (2006) 142–153 1015-1621/06/020142-12 DOI 10.1007/s00027-006-0818-5 Aquatic Sciences © Eawag, Dübendorf, 2006 Research Article Can algal photosynthetic inorganic carbon isotope fractionation be predicted in lakes using existing models? Darren L. Bade1,3,*, Michael L. Pace2, Jonathan J. Cole2 and Stephen R. Carpenter1 1 Center for Limnology, University of Wisconsin-Madison, USA 2 Institute of Ecosystem Studies, Millbrook, NY, USA 3 Present address: Institute of Ecosystem Studies, PO Box AB (65 Sharon Turnpike), Millbrook, NY 12545, USA Received: 30 June 2005; revised manuscript accepted: 7 December 2005 Abstract. Differential fractionation of inorganic carbon stable isotopes for studies ranging from food webs to stable isotopes during photosynthesis is an important paleolimnology. In our largest comparative study, values cause of variability in algal carbon isotope signatures. of δ13C-POC ranged from –35.1 ‰ to –21.3 ‰. Using Several physiological models have been proposed to ex- several methods to obtain an algal isotopic signature, we ε plain algal photosynthetic fractionation factors ( p). These found high variability in fractionation among lakes. There ε models generally consider CO2 concentration, growth was no relationship between p and one of the most im- rate, or cell morphometry and have been supported by portant predictors in existing models, pCO2. A whole-lake empirical evidence from laboratory cultures. Here, we inorganic 13C addition was used to create distinct algal ε explore the applicability of these models to a broad range isotope signatures to aid in examining p. Measurements of lakes with mixed phytoplankton communities. Under- and a statistical model from the isotope addition revealed standing this fractionation is necessary for using carbon that algal fractionation was often low (0 – 15 ‰). Key words. Photosynthetic fractionation; carbon stable isotopes; algae; particulate organic carbon; lakes. Introduction or CO2 concentrations (Oana and Deevey, 1960; Hol- lander and McKenzie, 1991; Schelske and Hodell, 1995; Fractionation of carbon isotopes during photosynthesis is Meyers and Lallier-Verges, 1999). Aquatic food web a key parameter for understanding organic carbon iso- studies utilize models of photosynthetic fractionation to tope signatures in aquatic ecosystems. Models of algal determine the isotope signature of phytoplankton, one photosynthetic fractionation have served as components important base of aquatic food webs (Karlsson et al., of some paleolimnological and aquatic food web studies. 2003; Pace et al., 2004). Paleolimnological studies benefi t from fractionation During photosynthesis, plants preferentially acquire models, because with the models and with measurement the lighter carbon isotope, 12C. Consequently, plant or- of the isotope signatures of sedimented algal material it ganic matter has a lighter isotope ratio than the source may be possible to reconstruct past levels of productivity inorganic carbon. Photosynthetic fractionation of carbon isotopes can occur at the diffusion, dissolution and car- boxylation steps. For land plants, differences among photosynthetic pathways (C , C and CAM) result in * Corresponding author phone: +1 845 677 5343; 3 4 fax: +1 845 677 5976; e-mail: [email protected] unique isotopic signatures among different types of Published Online First: May 30, 2006 plants, and water use effi ciency may cause some varia- Aquat. Sci. Vol. 68, 2006 Research Article 143 tion within types (Lajtha and Michener, 1994). For C3 based on isotopic measurements of dissolved inorganic photosynthesis (a common pathway of terrestrial and carbon (DIC), particulate organic carbon (POC) and size- aquatic photosynthesis) most of the fractionation occurs separated POC, across a gradient of lakes. We made during carboxylation of CO2, and for the enzyme RU- similar measurements during an experimental inorganic BISCO this fractionation may be near –25 ‰ to –28 ‰ in carbon isotope manipulation in two lakes to assess tem- ε algae (Goericke and Fry, 1994; Popp et al., 1998). If dif- poral variability in p. Although mechanisms represented fusion of CO2 into the cell becomes rate limiting (i.e. if in laboratory models are important, our results indicate CO2 concentration is low), then the fractionation during there are many complicating factors that prevent general carboxylation will become minimal. Diffusion of CO2 is use of these existing models for phytoplankton commu- slower in water than in air, thus the decline from the nities in lakes. Investigators should instead consider maximal fractionation is observed frequently in aquatic measuring algal carbon isotopes directly. plants, especially benthic algae (Finlay et al., 1999). Early observations of the photosynthetic fractionation ε factor ( p) in algae found a relationship between external Methods ε CO2 concentrations and p (Rau et al., 1989). Later, work- ers recognized the possibility of an inverse relationship Total POC comparative study ε between p and µ/[CO2], where µ is the growth rate of the Two separate comparative studies were conducted. The algae (Francois et al., 1993; Laws et al., 1995). Cell ge- fi rst involved collection of whole water POC for isotope ometry also explained some of the species-specifi c dif- analysis and the second involved collection of specifi c ε ferences observed in the p versus µ/[CO2] relationship size fractions of POC for isotope analysis. For the fi rst (Popp et al., 1998). study, surface waters (1m depth) were sampled in 32 Other factors also affect the photosynthetic fractiona- temperate lakes in the Northern Highland region of – tion by algae. Some algae have the ability to use HCO3 in northern Wisconsin and the Upper Peninsula of Michigan – addition to CO2 (Raven, 1970). Since HCO3 has a greater during the summer of 2000. The lake water was pre-fi l- 13 ε δ13 affi nity for C, the apparent fractionation ( p = CO2- tered through 153-µm mesh to remove large zooplankton, δ13algae) will be smaller. However, present models are and POC was collected on pre-combusted 25-mm What- – not able to discern whether CO2 or HCO3 is the source of man GF/F fi lters and dried at 60 °C for at least 48 h. Fil- inorganic carbon, and whether it is taken up passively or ters were fumed with HCl prior to analysis to remove actively (Laws et al., 1997; Keller and Morel, 1999). The inorganic carbon. The University of Alaska-Fairbanks presence of a carbon concentrating mechanism has been Stable Isotope Facility conducted C isotopic analysis of proposed for some algae, and this mechanism has been the POC using a Carlo Erba Elemental Analyzer, a Finni- shown to reduce fractionation (Sharkey and Berry, 1985). gan MAT Confl o II/III interface with a Delta+ mass spec- Finally different photosynthetic pathways in land plants trometer. Samples for 13C-DIC (dissolved inorganic car- (C3, C4, and CAM) fractionate carbon distinctively. bon) were collected in 1 L amber glass bottles and Analogously, carboxylation by enzymes other than RU- preserved at pH < 2 with 1 ml 10 N H2SO4. The samples BISCO within aquatic algae could lead to differences in were stored in the dark until they were sent to the Marine the degree of fractionation observed (Falkowski, 1991). Biological Laboratory, Woods Hole, MA for isotope Although models of photosynthetic fractionation analysis. Other limnological sampling of these lakes is have seldom been tested in natural freshwater environ- given by Bade et al. (2004). Of interest for this study are ments (Yoshioka, 1997; Finlay, 2004), their use has been the partial pressure of CO2 (pCO2), and Chl. a. CO2 par- relatively widespread in aquatic ecology. However, there tial pressures were measured with the headspace equili- is some indication that these models may not be appro- bration technique (Cole et al., 1994). Chl. a was collected priate in all freshwater situations since fractionation ap- on 47-mm Whatman GF/F fi lters, frozen, and extracted pears to be less than would be predicted based on these with methanol; concentrations were measured fl uoro- models (Cole et al., 2002; Pace et al., 2004). Also, it is metrically with corrections for pheopigments (Marker et increasingly recognized that for marine algae these mod- al., 1980). Chl. a samples were not pre-fi ltered through els are not applicable to all species, and that differing 153-µm mesh, unlike the POC samples. Several lakes ε growth limitation may also infl uence p (Rau et al., 1989; were sampled multiple times throughout the summer. Burkhardt et al., 1999a, b). These were considered independent samples in statistical ε This study examines estimates of p in freshwater analysis. lakes. Our goal is to determine if the general patterns Sestonic POC is a mixture of material, including al- ε found in laboratory estimates of p apply to freshwater gae and terrestrial detritus (del Giorgio and France, 1996; ecosystems with diverse and mixed algal species. Spe- Hessen et al., 2003). We calculated the signature of the cifi cally we investigate if CO2 or CO2 and growth rate are algal portion by using a two end-member mixing model ε ε suitable for predicting p among lakes. We examine p of the form: 144 D. L. Bade et al. Photosynthetic isotopic fractionation in algae δ13algae = (δ13POC[POC] – δ13terr[terr]) / [algae]. (1) mesh sizes of 45-µm and 20-µm were also used. The ma- terial collected on the mesh was examined qualitatively The mass of the algal component, [algae], was calculated under a microscope for the presence of non-algal mate- by using the measured amount of Chl. a and multiplying rial immediately after collection, or refrigerated and ex- by an assumed algal-C:Chl ratio of 40 (by mass). The amined within one day. The size fractions that were cho- remainder of the mass of POC, [POC], was considered to sen for isotope analyses consisted mostly of material that be terrestrial detritus, [terr] = [POC] – [algae]. The non- could be identifi ed as algal, and only a small proportion algal component was assumed to have an isotope signa- of unidentifi able amorphous material.
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