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Life-Forms of Phytoplankton As Survival Alternatives in an Unstable

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Life-Forms of Phytoplankton As Survival Alternatives in an Unstable ______________________________________o_c_EA_N_O __ LO_G __ IC_A_A_C_T_A __ 19_7_8_-_v_o_L_._1_-_N_ 0_4~~~---- Life-forms Phytoplankton Life-forms Turbulence Diatoms Dinoftagellates Types biologiques of phytoplankton Phytoplancton Turbulence Diatomées as survival alternatives Dinoftagellés in an unstable environment Ramon Margalef Departamento de Ecologia, Universidad de Barcelona, Barcelona, 7, Spain. Received 4/4/78, in revised form 20/5/78, accepted 28/5/78. The different life-forms observed in phytoplankton are functionally interpreted as adap­ ABSTRACT tations to survival in an unstable and turbulent environment. In comparison with terres­ trial and benthic plants, the primary producers in phytoplankton are small, of rapid turnover and expendable; this is the result of evolution under conditions of automatic and passive exploitation, where grazing may be only secondary. Any atom is more likely to travel downwards when in a particle than in solution, and the most likely final situation in a completely stagnant environment would be one of segregation between light (on top) and nutrients (in depth). Stability and local diversification on different scales may be interpreted in the same manner. The combination of sedimentation with turbulence or variance in the components of velocity is believed to be the most important factor in the biology of phytoplankton. Consequent! y, the best predictor of primary production and of dominant life-forms in phytoplankton is the available externat energy, on which advection and turbulence depend. This factor overrules more detailed models using light and nutrients as most relevant parameters, and based on laboratory experiments. Energy controls transportation, although the motility of organisms also contributes to the vertical organization of the ecosystem. The amount of energy exchanged and degraded per unit of surface also finds expression in the horizontal dimension of the structures that may be studied as approximatively closed systems with reference to the cycle of matter. Comparative analysis of different life-forms and their relation to the properties of the environment leads to an ordination along a main sequence, from fertile and turbulent water to exhausted and stratified environments. Populations selected under such diverging conditions range typically from diatoms to dinofiagellates. This correspondence is explained with the help of the model of Riley et al. ( 1949), which may be further developed in different ways. Fresh waters considerably expand the niche space of phytoplankton over the area of specially enriched water, and in such conditions cells enveloped in mucilage are frequent in a life-form not altogether absent in marine phytoplankton. Interpretation of such covers in terms of selection is not completely satisfactory, but mucilaginous envelopes of this type retard absorption and act as a feedback mechanism of population control. lt is possible to balance in a single expression environmental factors and properties of the organisms, in such a way that probability of survival might be inferred from sorne performance index computed on such variables. Oceanol. Acta, 1978, 1, 4, 493-509 RÉSUMÉ Les types biologiques du phytoplancton, considérés comme des alternatives de survte dans un milieu instable Les caractéristiques des différents types biologiques reconnaissables dans le phyto­ plancton sont interpré~ées fonctionnellement comme des adaptations à la survie dans un milieu essentiellement instable, turbulent. Contrairement aux producteurs primaires terrestres-et benthiques, les algues du plancton sont petites, à renouvellement rapide, 493 R. MARGALEF et subissent des pertes inévitables, dans lesquelles l'effet des animaux ne vient qu'en seconde place. Tout élément chimique a une plus grande probabilité de migrer vers le fond s'il est associé à une particule que s'il est un des constituants d'une substance dissoute; en conséquence, la situation finale la plus probable est une dissociation entre la lumière (couches supérieures) et les éléments nutritifs (accumulés dans les couches profondes). Le même processus, responsable du ralentissement des cycles et de la stabi­ lisation, peut se moduler avec plus de détail. La probabilité de sédimentation, combinée avec la variance des composantes des vitesses dans les différentes dimensions, est regardée comme le principal facteur qui régit la biologie du phytoplancton. L'énergie externe dont la dégradation nourrit l'advection et la turbulence, permet la meilleure prédiction de la production primaire et des types biologiques qui survivent. L'énergie échangée définit aussi la dimension horizontale des structures qui peuvent être étudiées comme des systèmes relativement clos en ce qui concerne la matière. L'énergie externe contrôle le transport, mais le mouvement propre des organismes contribue aussi à l'organisation verticale de l'écosystème. Les modèles détaillés de la biologie du phytoplancton, basés sur les effets, étudiés au laboratoire, de la lumière et de la concentration en sels nutritifs. ont leur utilité; leur possibilité d'application pratique est cependant limitée en raison du rôle prépondérant des mouvements de l'eau. L'analyse des rapports entre les pro­ priétés du milieu et les types biologiques permet de reconnaître une séquence principale qui va des eaux fertiles et turbulentes aux eaux pauvres et stratifiées et correspond à un classement des organismes, dont les formes typiques extrêmes sont, respectivement, les diatomées et les dinoflagellés à cellule aplatie. Leur morphologie s'explique fonc­ tionnellement sur la base du modèle de Riley et al. (1949) qui peut être un point de départ utile. Le phytoplancton des eaux douces montre un enrichissement de types biologiques dans les milieux spécialement concentrés en éléments nutritifs. Un type biologique caractéristique qui, quoique rare, ne manque pas dans le milieu marin, possède des enveloppes mucilagineuses, diversement interprétées, mais qui certainement ont pour effet de ralentir l'absorption des éléments nutritifs, et peuvent représenter ainsi un méca­ nisme de régulation des populations. Il est possible d'unir dans une seule expression des paramètres concernant les organismes et d'autres caractérisant leur milieu, de façon à pondérer un indice total, exprimant la probabilité de persistance de la combinaison envisagée dans chaque cas. Oceanol. Acta, 1978, 1, 4, 493-509. INTRODUCTION the number of molecules of chlorophyll and the number of centres of reaction in the chloroplast. A comparable The purpose of this paper is to examine the selection dead end appears at another level of organization in processes leading to different life-forms of phytoplankton, terrestrial plants, in the form of constructional limita­ as alternative strategies for survival. In plankton eco­ tions in the section of transport tissue. In practice, systems, the survival of populations is the result of an upper limit of productivity is set by the self shading a temporary equilibrium between success in remaining effect of chlorophyll. An optical density of 2, that is, afloat and inevitable sinking. This process will be exa­ the absorption of 99% of the incident light, is achieved mined in broad terms with reference to marine phyto­ by little more than 300 mg of chlorophyll per square plankton, with frequent utilization of hints and elues metre, that is, by a single sheet of Ieaves on land. by provided by the study of freshwater communities. the equivalent of a single layer or of a few layers of This is a subject of general ecology that requires sorne cells in water. On earth, the ratio between the extension excursions in peripheral fields. Such ancillary material, of leaves (maximal section) and the surface of soi! on unless referenced, is based on Margalef (1974 b). which the vegetation stands is, on the average, 4. 3 Horn (1971, p. 123) writes that "the most productive (Lieth and Whittaker, 1975), and this means that the community would be an infinitude of layers of sparse amount of available chlorophyll is four times that which and microscopie leaves with no non productive suppor­ can be effectively operating. The concentration of ting tissue. Phytoplankton in turbulent water form such chlorophyll in plankton rarely attains the limit of optical a community ". But is this really so? Terrestrial eco­ density 2; the most commonly observed concentrations 2 systems are in fact, on the average, three times more are between 5 and lOO mg/m • productive per unit surface than aquatic systems. This is Organization of the phytoplankton community is related a natural consequence of the "bottomless" (eu)photic to the extinction of light in water. Terrestrial vegetation layer in water. grows at the bottom of the atmosphere; aquatic vege­ The basic, built in limitation in primary production, tation in the top layers of water. The distribution of valid for the entire biosphere, lies in the ratio between phytoplankton chlorophyll could be compared against 494 LIFE-FORMS OF PHYTOPLANKTON an ideal distribution that optimizes the absorption of In experimental ecology, the reactions of an organism light by the plants, taking into account other causes of or of a population to different intensities or concen­ extinction by water and miscellaneous dissolved and trations of each of the factors under test are observed. suspended materials. If (chi) is the concentration of The factor may be declared to be important if there chlorophyll, k' its absoption per unit concentration, is a significant correspondence between
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