Size scaling deviation in phytoplankton photosynthesis and the energy flow through a
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1 ICES CM2004/Q:04 Size scaling deviation in phytoplankton photosynthesis and the energy flow through a coastal ecosystem. Pedro Cermeño, Emilio Marañón, Jaime Rodríguez, Emilio Fernández, Francisco Jiménez and Laura Zabala. ICES Recent Advances in the Oceanography and Biology of the Iberian Waters and Adjacent Shelf Seas: Results from Integrated Multidisciplinary Projects. ICES CM2004/Q:04. XXpp. We obtained a total of 50 abundance and photosynthesis size spectra during a full annual cycle from July 2001 to July 2002 in a coastal upwelling ecosystem. On average, the slope of the size abundance spectrum was 0.82 ± The size spectrum of cellspecific photosynthesis showed an average slope of 1.13 ± 0.36, which is significantly higher than 0.75 predicted by the size scaling theory. Assuming that phytoplankton respiration is independent of cell size, our results indicate that larger phytoplankton have higher growth rates than smaller cells do. The combination of abundance and cellspecific photosynthesis size spectra suggests that larger phytoplankton utilize a disproportionately large share of the resources within the ecosystem. The implication of these results is that an allometric deviation of the phytoplankton photosynthesis from overall allometric rules, rather than size-differential biomass accumulation, is the major responsible for a higher contribution of large sized phytoplankton to the total primary production. 1
2 Keywords: Phytoplankton, abundance, photosynthesis, cell size, energy flow. Pedro Cermeño, Emilio Marañón and Emilio Fernández: Departamento de Ecología y Biología Animal, Facultad de Ciencias del Mar, Universidad de Vigo, Vigo, Spain; tel: ; fax: Jaime Rodríguez, Francisco Jiménez and Laura Zabala: Departamento de Ecología y Geología, Universidad de Málaga, Campus de Teatinos, Málaga, Spain; tel: Correspondence to Pedro Cermeño: pca@uvigo.es Introduction The importance of coastal upwelling regions has long been recognised, both because they sustain large stocks of exploited living resources and also because of their potential to act as net sinks of atmospheric carbon (Ryther, 1969; Walsh, 1991). Upwelling events supply nutrients to the euphotic layer, enhancing primary production and shaping the size structure of plankton communities. It is well known that in these ecosystems the phytoplankton community is dominated by large sized cells, both in terms of biomass and productivity. This dominance has a great impact on the biogeochemical functioning of these ecosystems since it determines their potential ability to export carbon to higher trophic levels and adjacent ecosystems (Legendre and Le Fèvre, 1989). But what causes the dominance of large sized phytoplankton in these productive, upwelling regions? Phytoplankton metabolism has typically been reported to scale as a cell size raised to the 0.75 power (Eppley and Sloan, 1966; Peters, 1983), meaning that large phytoplankton 2
3 have lower growth rates than smaller cells. This is why the dominance of larger phytoplankton has traditionally been related to trophic mechanisms, in particular the temporal and spatial uncoupling between large phytoplankton and mesozooplankton (i. e. with longer generation times than those of phytoplankton), which gives rise to the accumulation of large sized cells (Banse, 1992). However, there exist numerous studies suggesting that larger phytoplankton, mainly diatoms, have higher photosynthetic efficiencies (i. e. chlorophyll-specific photosynthesis) than smaller cells (i.e. Legendre et al., 1993; Hashimoto and Shiomoto, 2002). This raises the possibility that a size scaling deviation in phytoplankton photosynthesis accounts for a higher contribution of large sized cells to the total phytoplankton photosynthesis. In this work, we determined the size spectra of phytoplankton abundance by concurrently using flow cytometry and microscopy image analyses in a coastal station at Ría de Vigo (NW Iberian Peninsula). Simultaneously, we also determined the photosynthesis rate by phytoplankton in four size fractions: picoplankton (<2 µm), small nanoplankton (2-5 µm), large nanoplankton (5-20 µm) and microplankton (>20 µm). Then, we combined the size scaling relationships of abundance and individual metabolism in order to obtain the size spectrum of community photosynthesis. Our main goal was to test the hypothesis that in coastal upwelling ecosystems purely physiological mechanisms may be responsible for the major contribution of larger cells to total phytoplankton photosynthesis. Methods 3
4 A total of 25 cruises to a central station in the Ría de Vigo (NW Iberian Peninsula; 'N 'W) were carried out from July 2001 to July 2002 on board RV `Mytilus. On each visit, a SeaBird CTD probe was used to obtain vertical profiles of temperature and salinity. Biological determinations were carried out at five sampling depths within the euphotic layer. Identification of phytoplankton and determination of their size and abundance were accomplished by using flow cytometry and microscopy image analyses. Flow cytometry and image analysis analytical subranges were coupled in order to obtain a sizeabundance spectrum of the whole phytoplankton community. Size-fractionated (0.2-2, 2-5, 5-20 and >20 µm) primary production was measured by conducting simulated in situ 14 C incubations that started at noon and lasted for 2 hours. For each size class, the average cell size was determined as the weighted cell abundance along the size spectrum. Mean cell volume was transformed to cell carbon biomass applying a biovolume to carbon conversion factor (Verity et al., 1992). Results Phytoplankton abundance varied by one-fold (from to cells ml -1 ) throughout our survey. On average, the size abundance spectrum (SAS) for the whole dataset showed a slope of 0.82 ± 0.27 (Fig. 1). Analyzing independently the dataset for each sampling day, our results indicated that the slope of the SAS ranged from 0.6 to 1 throughout the survey. Less negative exponents were observed during highly productive upwelling-stratification sequences and more negative exponents during winter mixing. 4
5 On average, cell-specific photosynthesis for the whole dataset increased as a power function of cell size with an exponent of 1.13 ± 0.36 (Fig. 2), which is significantly higher than 0.75 predicted by overall allometric rules. Similarly to the slope of the SAS, the size scaling exponent of phytoplankton photosynthesis showed a high degree of seasonal variability with higher values during upwelling-stratification sequences and lower values during winter mixing. Discussion The size scaling exponent of phytoplankton photosynthesis presented in this work reflects an interesting feature of coastal upwelling ecosystems. Assuming sizeindependent respiration rates of phytoplankton (Banse, 1976), our results indicate that large sized phytoplankton grow faster than small sized cells. This finding contrasts with the overall size scaling theory which predicts a 3/4 power relationship (Peters, 1983). However, different studies have reported a strong interspecific variability in the massspecific photosynthesis of phytoplankton (Chisholm, 1992). As an example, it is well known that diatoms have higher maximum growth rates than flagellates of the same size (Banse, 1982; Furnas, 1990). Analyses to address this question have focused on group specific metabolic strategies or resource allocation patterns. Thus, it is conceivable that although geometric constraints, such as the surface to volume (S/V) ratio in phytoplankton, are the basis from which allometric rules stem (Peters, 1983), however taxon-related physiological strategies may account for the high size scaling exponent of phytoplankton photosynthesis found in this work. Using the size scaling relationships of abundance (N, in units of cels ml -1 ) and 5
6 metabolism (R, in units of fg C cel -1 h -1 ) obtained in this study, we determined the size scaling exponent of the relationship between the photosynthesis per unit volume (Q tot, in units of fg C ml -1 h -1 ) and the cell size (in this equation cell size is denoted as M, in units of pg C cel -1 ): Q tot = N R M 0.8 M 1.1 M 0.3 Our results indicated that at the community level of organization most of the photosynthesis is accounted for by larger phytoplankton. This result is consistent with traditional biogeochemical models of coastal upwelling regions which predict a short, classical food web, characterized by the export of large celled phytoplankton to higher trophic levels and adjacent ecosystems (Legendre and Le Fèvre, 1989). It has to be taken into account that our measurements of metabolic rates and organism densities do not account for the same temporal and spatial scales of variability. Photosynthesis estimates represent an instantaneous rate of carbon assimilation by the whole phytoplankton community. In contrast, the size-abundance distributions of phytoplankton assemblages reflect a series of processes taking place over longer time scales (i. e. size-differential loss rates) (Tremblay and Legendre, 1994). If we interpret both metabolism and abundance size spectra (Figs. 1 and 2) on similar time scales, the size scaling deviation of phytoplankton photosynthesis appears to be strongly inconsistent with the slope of the SAS (i.e. we would expect a less negative slope in the latter), suggesting an active exportation of phytoplankton biomass. This discrepancy between the size spectra of metabolism and abundance strongly indicates that the size scaling deviation of phytoplankton photosynthesis, rather than size-differential biomass 6
7 accumulation, accounts for the major contribution of large sized phytoplankton to total photosynthesis in coastal upwelling ecosystems. Despite the robustness and widespread use of the size scaling theory, demonstrated over a wide range of organism sizes and across different phyla, size scaling deviations of metabolism from theoretical expectations emerge as a result of taxon-specific abilities or constraints of the organisms when coping with different environmental conditions. In this work, we have shown that an allometric deviation of phytoplankton photosynthesis accounts for the higher contribution of large sized phytoplankton to the total community metabolism. The optimization of nutrients pulses by diatoms is likely to be a major mechanism responsible for a size scaling deviation of phytoplankton photosynthesis from overall allometric expectations. This result indicates that within local ecosystems the size scaling analysis of metabolism may provide fundamental patterns of resource allocation which differ from theoretical predictions. These patterns are critical in determining the ecological and biogeochemical functioning of planktonic ecosystems. Acknowledgements. P. C. was supported by a postgraduate research fellowship from the Spanish Ministry of Science and Technology (MCYT). This research was funded by MCYT through research grant REN to E.M. 7
8 References: Banse, K Rates of growth, respiration and photosynthesis of unicellular algae as related to cell size a review. Journal of Phycology. 12: Banse, K Cell volumes, maximum growth rates of unicellular algae and ciliates, the role of ciliates in the marine pelagial. Limnology and Oceanography, 27: Banse, K Grazing, temporal changes of phytoplankton concentrations, and the microbial loop in the open sea. pp In P. G. Falkowski and A. D. Woodhead [eds.], Primary productivity and biogeochemical cycles in the sea. Plenum. Chisholm, S. W Phytoplankton size, pp In P. G. Falkowski and A. D. Woodhead [eds.], Primary productivity and biogeochemical cycles in the sea. Plenum. Eppley, R. W., and Sloan, P. R Growth rates of marine phytoplankton: Correlation with light absorption by cell chlorophyll a. Physiologia Plantarum, 19: Furnas, M. L In situ growth rates of marine phytoplankton: approaches to measurement, community and species growth rates. Journal of Plankton Research, 12: Hashimoto, S., and Shiomoto, A Light utilization efficiency of size-fractionated phytoplankton in the subartic Pacific, spring and summer 1999: high efficiency of largesized diatom. Journal of Plankton Research, 24: Legendre, L., Gosselin, M., Hirche, Hj., Kattner, G., and Rosenberg, G Environmental control and potential fate of size fractionated phytoplankton in the Greenland Sea (75º N). Marine Ecology Progress Series, 98: Legendre, L., and Le Fevre, J Hydrodynamical singularities as controls of recycled versus export production in oceans. In: Productivity of the ocean: present and past. W. H. Berger [ed], Wiley, New York. pp Peters, R. H The ecological implications of body size. Cambridge Univ. Press. Ryther, J. H. (1969). Photosynthesis and fish production in the sea. Science, 166: Tremblay, J. E. and Legendre, L A model for the size-fractionated biomass and production of marine phytoplankton. Limnology and Oceanography, 39: Verity, P. G., Robertson, C. Y., Tronzo, C. R., Andrews, M. G., Nelson, J. R., and Sieracki, M. E Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnology and Oceanography, 37: Walsh, J. J Importance of continental margins in the marine biogeochemical cycling of carbon and nitrogen. Nature, 350:
9 Figure Legends: Figure 1. Relationship between phytoplankton abundance (in units of cels ml -1 ) and cell size (in units of pg C per cell) obtained from a total of 50 seawater samples collected from July 2001 to July Open and closed circles are for surface and 10 m depth, respectively. Solid line represents Model II linear regression (n=743) after applying a logarithmic transformation to both variables [log cell abundance = 2.4 (± 0.64) 0.82 (± 0.27) log size, r 2 = 0.89, p<0.0001]. Figure 2. Relationship between cell-specific photosynthesis (in units of fg C cell -1 h -1 ) and average cell size (in units of pg C cell -1 ). All data are for phytoplankton assemblages in surface waters and 10m depth from July 2001 to July Symbols are as in Fig. 1. Solid line represents Model II linear regression (n=192) after applying a logarithmic transformation to both variables [log cell-specific photosynthesis = 13.4 (± 0.62) (± 0.36) log size, r 2 = 0.89, p<0.0001]. 9
10 Figure 1. Cermeño et al. Cell abundance (cells ml-1) Cell carbon mass (pg C per cell) Figure 2. Cermeño et al. Cell-specific photosynthesis (fg C cel -1 h -1 ) Cell carbon mass (pg C per cell) 10
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