Nutrient Limitations, Microbial Food Webs, and 'Biological C-Pumps': Suggested Interactions in a P-Limited Mediterranean
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MARINE ECOLOGY PROGRESS SERIES Published February 9 Mar. Ecol. Prog. Ser. 1 REVIEW Nutrient limitations, microbial food webs, and 'biological C-pumps': suggested interactions in a P-limited Mediterranean T. Frede ~hingstad',Fereidoun Rassoulzadegan2 'Department of Microbiology, University of Bergen, Jahnebakken 5, N-5020 Bergen, Norway Station Zoologique, BP 28, F-06230 Villefranche-sur-Mer, France ABSTRACT: In light of evidence suggesting that both phytoplankton and bacteria in the Medi- terranean Sea are limited by the availability of phosphorus rather than of nitrogen, and that most of the P in the photic zone during summer stratification exists as dissolved organic compounds (DOP),we address the question of how these observations may interact with the 'biological pump' transporting carbon to deep waters. From theoretical considerations, the C storage via sinking particles should func- tion better in a P- than in an N-hted system. It is argued, however, that the microbial food web dur- ing summer stratification has a net accumulation of dissolved organic carbon (DOC) and DOP. The hm- ited data available suggest a high DOC : DOP value which would make downwards transport of DOC with winter deep water formation a potentially effective mechanism in C sequestration from the atmo- sphere. Part of the DOC accumulating in the photic zone appears to be readily biodegradable. This is in conflict with a simple model of phytoplankton-bacterial competition for phosphate since phyto- plankton, as an inferior competitor, would be expected to be reduced in biomass until autochthonous production of organic C falls to a level where bacteria become C-lmuted. The conflict is resolved by including microzooplankton grazing as a controlling factor of bacterial biomass. KEY WORDS: Phosphorus limitation Microbial food webs Carbon cycles . Marine biogeochemistry P-LIMITATION IN THE MEDITERRANEAN SEA? tions, there are several references suggesting that the relationships between P and N are special in the Considering (1)that the ratio of available nitrogen to Mediterranean Sea with larger probabilities of P be- phosphate in the western Atlantic seems to be close to coming limiting for primary production than usually the Redfield ratio of 16 (Richards 1958), and (2) that P observed in true marine systems. Berland et al. (1980) seems to be more rapidly recycled than N (Bishop et al. reviewed the available evidence and concluded that 1977, Martin et al. 1979, Garber 1984), a mechanism the Mediterranean seemed to be peculiar in having P suggested to lead to development towards N-limitation as the most limiting factor for primary production. in recycling ecosystems (McGill 1965, Hickel et al. More recently, Krom et al. (1991) measured the re- 1993), one might be led to expect that N-limitation of maining concentrations of inorganic nutnents and primary production during summer stratification of the found as a general trend an increasing N:P ratio east- Mediterranean should increase as nutrient-depleted wards in the Mediterranean. On the basis of high inor- surface water imported through the Straits of Gibraltar ganic N:P ratios, the Adriatic Sea has also been consid- is transported eastwards. Contrary to such specula- ered to be P-limited (Vukadin & Stojanski 1976),while 63 Inter-Research 1995 Resale of full article not permitted 300 Mar. Ecol. Prog. Ser. 117.299-306, 1995 McGill(1965),in a set of very variable N:P ratios, found quirements (Sakshaug & Holm-Hansen 1977, Parslow high values in the Ionian and Ligurian Seas. Nutrient et al. 1984) and induction of enzymes such as alkaline enrichment studies in the northwestern Mediterranean phosphatase (Perry 1972),may be taken as indicators support this general impression of a predominance of of a P-starvation of the individual cells. If this starva- P-limtation (Jacques et al. 1973, Fiala et al. 1976) but tion is strong enough to block processes essential for N and iron were found to play a role in parts of the growth such as DNA synthesis, one could speak of year. In contrast to this, Owens et al. (1989)concluded a 'physiological' P-limitation. Such 'physiological' that N-limitation was more probable than P-limitation nutrient limitation is closely linked to, but not identical in the western part. Coastal areas heavily influenced to, what might be called a 'systemic' nutrient limitation by freshwater such as the northern Baltic (Lignell et al. (Paasche & Erga 1988). 'Systemic' nutrient limitation 1992) and Norwegian fjords (Thmgstad et al. 1993),or would be the limitation on total biomass in the system by freshwater seasonally carrying large concentrations caused by the restricted amount of nucleic acids, pro- of nitrate from farmland runoff such as those off the terns or other essential cell components which can be North Sea coast of the European continent (Hickel et formed on the restricted amount of the nutrient avail- al. 19931, may become P- rather than N-limited. In the able. This type of limitation would be demonstrated Mediterranean Sea with its relatively low freshwater by a (temporary or permanent) increase in biomass input and high salinity, P-hmitation is difficult to following an addition of the limiting nutrient to the explain as a consequence of freshwater influence. system. The importance of sucha distinction in termi- Since nitrate : phosphate ratios in the Mediterranean nology may be illustrated by considering the paradox- deep waters are above the Redfield ratio, and appar- ical situation that phytoplankton in oligotrophic envi- ently have been so since early measurements (McGill ronments sometimes seem to grow at near-maximum 1965), neither redistribution mechanisms within the growth rates (Goldman et al. 1979). If, in accordance water column, nor recent changes in human influence with expectations, such an oligotrophic system re- such as P-removal from sewage, seem to offerexplana- sponds to added nutrients by an increase in biomass, it tions to the observed P-limitation rn the surface layer. would seem to be an example of 'systemic limitation' Other mechanisms such as fast N fixation rates m occurring without any appreciable 'physiological limi- coastal areas (Bethoux & Copin-Montegut 1986, tation'. Apparently (and interestingly),the implication Bethoux et al. 1992) or selective phosphate precipita- of the observed 'physiological limitation' in Ville- tion due to input of iron-containing dust from the franche Bay surface waters is that this environment Sahara (Krom et al. 1991) have been suggested. does not seem to conform to the Goldman paradox. The question of a possible P-limitation in the western The coupling between 'physiological' and 'systemic' part has recently been examined more closely through P-limitations may be illustrated by simple food chain investigations m VillefrancheBay on the French Medi- models of the type analyzed by Thingstad & Sakshaug terranean coast. Zweifel et al. (1993) demonstrated (1990)who suggested a model in which low total con- how orthophosphate addition would stimulate bac- centration (sumin all biological and biologically avail- terial growth and degradation of naturally occurring able pools) of the limiting nutrient in the photic zone dissolved organic carbon (DOC) in filtered (0.2 pm) would correspond to a food chain based on primary seawater reinoculated with bacteria. Also, orthophos- nutrient uptake in small-sized organisms, few predator phate addition seemingly stimulates DNA synthesis in levels with inefficientrecycling, and a strong 'physio- the native Synechococcus population (D.Vaulot pers. logical' limitation of the organisms doing the primary comm.). Other evidence such as high alkaline phos- uptake. Increased total concentration of available phatase activity, short orthophosphate turnover times, nutrient would shift the equilibrium towards more and a significant 'luxury consumption' in both the bac- predator steps with more recycling and less 'physio- terial and phytoplankton dominated size-fractions logical' nutrient limitation at the bottom of the food (Thingstad et al. unpubl.), all uniformly supports the chain and, at sufficientlyhigh total nutrient concentra- impression that both bacteria and phytoplankton expe- tion, to the introduction of larger primary producers. rience what might be called a 'physiological P-limita- Within such a framework, the signs of 'physiological' tion' (Paasche & Erga 1988). P-limitation at the bottom of the food cham as found in Villefranche Bay could be interpreted as signs of low concentration of biologically available total P, and EQUILIBRIUM CONDITIONS FOR THE therefore a short food chain where regeneration does PHOTIC ZONE FOOD WEB not satisfy the P-requirements of the standing stock of phytoplankton and bacteria. Some physiological processes such as orthophos- In an open system such as the oceanic photic zone, phate uptake far in excess of immediate growth re- there is of course the extra equilibrium condition of Thingstad & Rassoulzadegan: Nutrient mteractions m the Mediterranean 301 nutrient import ('newiproduction) equilibrating export when integrated over sufficienttime (Dugdale & Goer- ing 1967). As a corollary to this: the food chain has to adjust to a structure and length (number of trophic levels) where the interacting organisms produce a loss equal to the input (Thingstad & Sakshaug 1990). Sources of inputs of 'new' nutrients to a system with P-limitation may differfrom that in N-limited systems where atmospheric input of N (Dahl et al. 1987, Bethoux et al. 1992) and N fixation (Bethoux