Shape and size in phytoplankton ecology: do they matter?

Transcription

1 Hydrobiologia (2007) 578: DOI /s z PHYTOPLANKTON WORKSHOP Shape and size in phytoplankton ecology: do they matter? Luigi Naselli-Flores Æ Judit Padisák Æ Meriç Albay Ó Springer Science+Business Media B.V Abstract This paper summarises the outcomes of the 14th Workshop of the International Association of Phytoplankton Taxonomy and Ecology (IAP). The authors mostly addressed their contributions on the following topics: morphological and morphofunctional descriptors of phytoplankton, size and shape structure of phytoplankton related to different kinds of environmental variables and the role of morphological and physiological plasticity of phytoplankton in maintaining the (apparently) same populations under different environmental conditions. Case studies from different kinds of aquatic environments (deep and shallow lakes, reservoirs with different age, purpose and trophic state, floodplain wetlands mostly in the temperate region but also from subtropical and tropical ones) have Guest editors: M. Albay, J. Padisák & L. Naselli-Flores Morphological plasticity of phytoplankton under different environmental constraints L. Naselli-Flores (&) Dipartimento di Scienze Botaniche, University of Palermo, Via Archirafi, 38, I-90 Palermo, Italy J. Padisák Department of Limnology, Pannon University, P.O. Box 158, H-8200 Veszprém, Hungary M. Albay Istanbul University Faculty of Fisheries, Ordu Cad. No: 200, Laleli, Istanbul, Turkey shown that similar environmental forcing calls for similar morpho-functional properties even though the corresponding associations can be markedly different on species level. Keywords Morphological traits Morpho-functional descriptors Plasticity of phytoplankton Organisational levels Introduction It is widely accepted that there is no casualty in determining the form of organisms. The study of shape and dimensions of the living has interested human beings since the antiquity. Greek philosophers and naturalists were attracted by the widespread presence in Nature of constantly repeated morphological patterns. The so called golden ratio, for instance, has been again and again found to govern the shape of a variety of life-forms: from the spirals of shells to the disposition of the leaves around the branches or the position of apple seeds inside the fruit (Douady & Couder, 1992). Even our perception of what is beauty and ordered is strongly influenced by the extent of the presence of this proportion in natural or artistic objects (Godkewitsch, 1974) or even in music (Putz, 1995). Living organisms are subject to physical laws and processes and these act on their form and

2 158 Hydrobiologia (2007) 578: mould it. Starting from this point, D.W. Thompson in his masterpiece On growth and form, (1992, but originally published in 1917), provided a mathematical analysis of biological processes and suggested that the possibilities of shapes among living organisms are limited when compared to what Physics makes available; nevertheless, these are enough to determine at least three conditions as different as those permitting life to mammals, insects and bacteria. He also faced the problem of scales and separated those organisms where physical forces act either directly at the surface of their body, or otherwise in proportion to their surface, from those where these forces, and above all gravity, act on all particles and result in a force proportional to the mass or volume of the body. In synthesis, he pointed out the necessity to distinguish among the forces acting on organisms living at low and high Reynold s numbers. Among the organisms living at low Reynold s numbers, phytoplankton offers an amazing morphological diversity and all those involved in phytoplankton research have commonly observed that these organisms are present in various shapes and may express a quite high variability, both intra- and inter-specific, in their morphology. These features have been traditionally used just for taxonomic classification of organisms. Lewis (1976) was one of the first recognising the ecological value of morphological descriptors in phytoplankton in relation to uptake of light and nutrients and, as a result of, natural selection and competition. A few years later Margalef (1978) used life-forms as a determinant of seasonal succession of phytoplankton suggesting that morphological variability has an adaptive value directed toward the best fitting to environmental template. More recently, Reynolds (1997), explained in detail how the diverse ecological strategies adopted by phytoplankton can be related to differences in their morphology. In taxonomy, morphology has been traditionally used as a main feature for phylogenetic classification but phylogenetic classification of organisms often do not reflect their ecological functions (Salmaso & Padisák, 2007) and the recording of selected morphological descriptors can represent a useful tool to better understand their ecology and the environmental features of their habitats. This paper summarises the results achieved by the participants to the 14th Workshop of the International Association of Phytoplankton Taxonomy and Ecology where an attempt to focus attention on the Morphological variability of phytoplankton under different environmental constraints was done as well as the different approaches they used to face the theme. Papers in this volume bring examples from many kinds of aquatic environments: deep and shallow lakes, reservoirs with different age, purpose and trophic state, floodplain wetlands mostly in the temperate region but subtropical and tropical aquatic ecosystems are also included. Spectrum of morphological features and plasticity Many morphological features are still widely used in Linnaean taxonomy and the grouping of organisms based upon their affinities has survived intact through over two centuries of continuous refinements (Reynolds et al., 2002). These are, for example, length (L) and width (W) of single cells, L/W ratio, presence or absence of protuberances (e.g. spines, arms, tubercules), mucilage (that can also show variability in terms of thickness and form), as well as the number of cells in a colony and their dimensions and arrangement, etc. In some cases, morphological variability simply reflects the reproductive physiology of individual species (Sommer, 1998). However, it is frequently subject to environmental variability and ecosystem features. Nevertheless, there are only few morphological descriptors used exclusively by ecologists and used to relate form to function. A good example is the surface/volume (S/V) ratio that is allometrically related to physiological characteristics of organisms as well as to some environmental features. Complexity of phytoplankton forms varies in a wide range, from very complicate shapes, like a Staurastrum with ornamented cell walls wearing arms embedded in mucilage, to picoplanktic ellipsoids with very few easily recognisable morphological traits. Such variability of forms has to have an ecological meaning and the coexistence of differently shaped organisms should reflect the environmental variability of pelagic ecosystems. In natural

3 Hydrobiologia (2007) 578: environments, size and form selection is perhaps the strongest driving force shaping phytoplankton assemblages under variable environmental conditions (Morabito et al., 2007). Morphological plasticity and different organisation levels Adaptation to environmental constraints is a inherent feature of single organisms. O Farrell et al. (2007) observed strong decrease in number of aerotopes of Cylindrospermopsis raciborskii 72 h after removing macrophytes from experimental tanks as a response to alteration in light conditions and exemplifying physiological plasticity. Many other physiological mechanisms could be listed, however, only few of such environmental impulses manifest in morphological changes; an example can be spine formation of Scenedesmus after exposition to infochemicals released by daphnids (Van Donk, 1997). Morphological variability is recognisable both at population and assemblage level. In the first case, each of the morphological descriptors can change within the limits of maximum variance characteristic for that species. Such morphological plasticity is not restricted to complicated shapes. As shown by Jezberová & Komarková(2007) morphologically very similar strains of picocyanoprokaryotes have different ability to change their shape (enlenghtening in this case) when they were grown under different laboratory conditions. When the extent of any environmental parameter exceeds the morphological adaptive capacity of a single population, species replacement takes place offering further adaptation at a higher organisation level. In this case, morphological plasticity is understood at assemblage level. Dynamic aquatic environments support a large diversity of different sizes and shapes of species either present in the assemblages or as propagules ready to develop as the environmental template changes (Padisák, 1992). Cell and colony size, mucilage formation and coiling Of the broad range of morphological descriptors, contributors of this volume mainly explored the variations in cell or colony size, the role of mucilage formation and the significance of filament coiling. Cell size occupies a keystone position in the ecological and physiological behaviour of algae, being dependent on this parameter the growth as well the loss processes of phytoplankton (Morabito et al., 2007). In particular, phytoplankton cell and colony size structure play a major role for the physiological performance along the vertical light gradient (Kaiblinger et al., 2007) and influences single species sinking rates and nutrient uptake (Stoyneva et al., 2007). Importance of size will be addressed later. Another important morphological variation is also related to size and shape of mucilage surrounding many species of phytoplankton. As shown by Reynolds (2007) mucilage production may be good for density reduction, nutrient sequestration and processing, as well as a source of defence against grazing and digestion, and heavy metal exposition. Moreover, it may maintain a reducing microenvironment around the cells. Coiling is a morphological feature that is extensively used in Anabaena taxonomy besides it may influence sinking properties or grazing resistance of species (Padisák et al., 2003). Morphological responses to light and nutrient availability The need of exploiting resources under variable environmental conditions is probably one of the most important causes of intra- and interspecific morphological diversity in phytoplankton (Naselli-Flores & Barone, 2000). Entrainment in the mixed water column is one of the strategies used by phytoplankton to explore and exploit these resources and the extent of such entrainment largely depends on shape and size (Padisák et al., 2003). The effects of underwater light climate in shaping phytoplankton assemblages were analysed by O Farrell et al. (2007). They found a prevalence of small unicellular, non-flagellated organisms, thin filaments or small tabular colonies in light limited environments, whereas flagellated

4 160 Hydrobiologia (2007) 578: forms and larger organisms prevailed in wellilluminated ones. These results are in agreement with the findings of Naselli-Flores & Barone (2007) who observed significant relationships between the daily availability of underwater light and the dominant morphology in the assemblage of a hypertrophic Mediterranean reservoir. Thus, light availability is a major force shaping phytoplankton assemblages in eutrophic and hypertrophic environments. Conversely, efficiency in nutrient uptake is more relevant in oligotrophic and mesotrophic ones. As shown by Morabito et al. (2007), this efficiency largely depends on S/ V ratio. High values of this ratio are common in small sized organisms and are generally related to a better nutrient flux per unit volume and to a higher photosynthetic efficiency. Morphological responses to grazing As frequently reported in literature, grazing is one of the most widely explored environmental constraint on size and shape spectrum of phytoplankton. Stoyneva et al. (2007) elegantly showed that Eremosphaera in Lake Tanganyika increases in size without notable changes in S/V ratio to minimise grazing pressure exerted by copepods during the dry season. Seasonality of morphological variations and effects of perturbations Different stratification patterns along with different incomes of light and nutrients provide an annually recurrent physical and chemical scenario. Morphological variations of phytoplankton assemblages reflect this periodicity. As Kamenir et al. (2007) synthetically underlined, physics drives chemistry, which triggers the phytoplankton response. At a population level, this changes are shown by Stoyneva et al. (2007) with observations on Eremosphaera tanganyikae that showed a more complex behaviour driven by biological interactions together with the annual periodicity in physical forcing. Being Eremosphaera a big, non-motile chlorococcalean species, it can sustain abundant populations only in the season with a deep mixing. During wet season larger specimens are gradually selected by copepods grazing pressure on smaller ones. On an assemblage level, Naselli-Flores & Barone (2007) recorded similar morphological trajectories followed by phytoplankton even though depicted by a different specific assemblage (corresponding species pairs in 1991/1992: Ankyra-Monoraphidium, Peridiniopsis-Gymnodinium, straight morphotype of Anabaena-Planktothrix). Morabito et al. (2007) measured a coefficient of variation close or higher than 20% for cell volume, surface and greater axial linear dimensio (GALD) across the seasonal succession of phytolankton in Lake Maggiore as a consequence of annual environmental variability. Seasonality of morpho-functional groups was evidently shown by Salmaso & Padisák (2007) by comparing phytoplankton seasonal succession in two deep oligotrophic lakes. In spite of the different specific composition of their phytoplankton, these two lakes were surprisingly similar in the seasonal patterns based on their morpho-functional groups. These groups correlated much better to plots obtained from ordinations on species level than the groups based on higher taxa (i.e. at Order, Class or Division level). The examples quoted above clearly show that morphological traits are suitable indicators of regularities in seasonal patterns. However, they not only show regular periodicities but also reflects effects of perturbations or disturbances. According to Kamenir et al. (2007), modifications of size structure of operative taxonomic units (OTU) reflect environmental perturbations as did morpho-functional groups in Lake Stechlin when Planktothrix rubescens started to grow unexpectedly (Salmaso & Padisák, 2007). Management of lake water quality can be considered as a large scale human imposed perturbation on the existing system. As Dokulil et al. (2007) noted in the context of the oxbow lake Alte Donau, where management measure was mainly based on chemical treatment (Dokulil et al., 2000), changes from one stable state to another are associated with significant changes in size structure of phytoplankton. Accordingly, Naselli-Flores & Barone (2007) pointed out that the application of different management strategy

5 Hydrobiologia (2007) 578: in summer water use, mainly directed toward a modification of the physical environment (Naselli-Flores & Barone, 2005), can strongly affect the morpho-functional trajectories of phytoplankton assemblages in response to substantial changes in underwater light climate. The above examples offer the useful and practical opportunity to monitor water quality on the basis of size and shape of dominant phytoplankton instead of dealing with highly precise, but time consuming, taxonomic resolution. This gives the chance to use phytoplankton easily as a monitoring tool. References Dokulil, M. T., K. Teubner & K. Donabaum, Restoration of a shallow, ground-water fed urban lake using a combination of internal management strategies: a case study. Archiv für Hydrobiologie, Special Issue Advances in Limnology 55: Dokulil, M. T., K. Donabaum & K. Teubner, Modifications in phytoplankton size structure by environmental constraints induced by regime shifts in an urban lake. Hydrobiologia 578: Douady, S. & Y. Couder, Phyllotaxis as a physical self-organized process. Physical Review Letters 68: Godkewitsch, M., The golden section: an artifact of stimulus range and measure of preference. American Journal of Psychology 87: Jezberová, J. & J. Komárková, Morphometry and growth of three Synechococcus-like picoplanktic cyanobacteria at different culture conditions. Hydrobiologia 578: Kaiblinger, C., S. Greisberger, K. Teubner & M. T. Dokulil, Photosynthetic efficiency as a function of thermal stratification and phytoplankton size structure in an oligotrophic alpine lake. Hydrobiologia 578: Kamenir, Y., Z. Dubinsky & T. Zohary, Stable patterns in size structure of a phytoplankton species of Lake Kinneret. Hydrobiologia 578: Lewis, W. M., Surface/volume ratio: implication for phytoplankton morphology. Science 192: Margalef, R., Life forms of phytoplankton as survival alternatives in an unstable environment. Oceanologica Acta 1: Morabito, G., A. Oggioni, E. Caravati & P. Panzani, Seasonal morphological plasticity of phytoplankton in Lago Maggiore (N. Italy). Hydrobiologia 578: Naselli-Flores, L. & R. Barone, Phytoplankton dynamics and structure: a comparative analysis in natural and man-made water bodies of different trophic state. Hydrobiologia 438: Naselli-Flores, L. & R. Barone, Water-level fluctuations in Mediterranean reservoirs: setting a dewatering threshold as a management tool to improve water quality. Hydrobiologia 548: Naselli-Flores, L. & R. Barone, Pluriannual morphological variability of phytoplankton in a highly productive Mediterranean reservoir (Lake Arancio, Southwestern Sicily). Hydrobiologia 578: O Farrell, I., P. de Tezanos Pinto & I. Izaguirre, Phytoplankton morphological response to the underwater light conditions in a vegetated wetland. Hydrobiologia 578: Padisák, J., Seasonal succession of phytoplankton in a large shallow lake (Balaton, Hungary) a dynamic approach to ecological memory, its possible role and mechanisms. Journal of Ecology 80: Padisák, J., E. Soróczki-Pintér & Z. Rezner, Sinking properties of some phytoplankton shapes and the relation of form resistance to morphological diversity of plankton an experimental study. Hydrobiologia 500: Putz, J. F., The golden section and the piano sonatas of Mozart. Mathematics Magazine 68: Reynolds, C. S., Vegetation Processes in the Pelagic: A Model for Ecosystem Theory. Ecology Institute, Oldendorf/Luhe: 371 pp. Reynolds, C. S., Variability in the provision and function of mucilage in phytoplankton: facultative responses to the environment. Hydrobiologia 578: Reynolds, C. S., V. Huszar, C. Kruk, L. Naselli-Flores & S. Melo, Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research 24: Salmaso, N. & J. Padisák, Morpho-Functional Groups and phytoplankton development in two deep lakes (Lake Garda, Italy and Lake Stechlin, Germany). Hydrobiologia 578: Sommer, U., Growth and survival strategies of planktonic diatoms. In Sandgren, C. D. (ed.), Growth and Reproductive Strategies of Freshwater Phytoplankton: Cambridge University Press, Cambridge, Stoyneva, M. P., J.-P. Descy & W. Vyverman, Green algae in Lake Tanganyika: Is morphological variation a response to seasonal changes? Hydrobiologia 578: Thompson, D. W., On growth and form. Abridged edition by J. T. Bonner. Cambridge Univerity Press, 368 pp. Van Donk, E., Defenses in phytoplankton against grazing induced by nutrient limitation, UV-B stress and infochemicals. Aquatic Ecology 31: