Hydrobiologia (2007) 578:157–161
DOI 10.1007/s10750-006-2815-z
P H Y T O P L A N K T O N W O RK S H O P
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. 2007
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-90123
Palermo, Italy
e-mail: [email protected]
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, 34470 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
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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
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Hydrobiologia (2007) 578:157–161
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
Hydrobiologia (2007) 578:157–161
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
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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
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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
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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
Hydrobiologia (2007) 578:157–161
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, 2000.
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: 271–282.
Dokulil, M. T., K. Donabaum & K. Teubner, 2007.
Modifications in phytoplankton size structure by
environmental constraints induced by regime shifts
in an urban lake. Hydrobiologia 578: 59–63.
Douady, S. & Y. Couder, 1992. Phyllotaxis as a physical
self-organized process. Physical Review Letters 68:
2098–2101.
Godkewitsch, M., 1974. The golden section: an artifact of
stimulus range and measure of preference. American
Journal of Psychology 87: 95–103.
Jezberová, J. & J. Komárková, 2007. Morphometry and
growth of three Synechococcus-like picoplanktic
cyanobacteria at different culture conditions. Hydrobiologia 578: 17–27.
Kaiblinger, C., S. Greisberger, K. Teubner & M. T.
Dokulil, 2007. Photosynthetic efficiency as a function
of thermal stratification and phytoplankton size
structure in an oligotrophic alpine lake. Hydrobiologia 578: 29–36.
Kamenir, Y., Z. Dubinsky & T. Zohary, 2007. Stable
patterns in size structure of a phytoplankton species of
Lake Kinneret. Hydrobiologia 578: 79–86.
Lewis, W. M., 1976. Surface/volume ratio: implication for
phytoplankton morphology. Science 192: 885–887.
Margalef, R., 1978. Life forms of phytoplankton as survival
alternatives in an unstable environment. Oceanologica Acta 1: 493–509.
Morabito, G., A. Oggioni, E. Caravati & P. Panzani, 2007.
Seasonal morphological plasticity of phytoplankton in
Lago Maggiore (N. Italy). Hydrobiologia 578: 47–57.
Naselli-Flores, L. & R. Barone, 2000. Phytoplankton
dynamics and structure: a comparative analysis in
161
natural and man-made water bodies of different
trophic state. Hydrobiologia 438: 65–74.
Naselli-Flores, L. & R. Barone, 2005. Water-level fluctuations in Mediterranean reservoirs: setting a dewatering threshold as a management tool to improve water
quality. Hydrobiologia 548: 85–99.
Naselli-Flores, L. & R. Barone, 2007. Pluriannual morphological variability of phytoplankton in a highly
productive Mediterranean reservoir (Lake Arancio,
Southwestern Sicily). Hydrobiologia 578: 87–95.
O’Farrell, I., P. de Tezanos Pinto & I. Izaguirre, 2007.
Phytoplankton morphological response to the underwater light conditions in a vegetated wetland. Hydrobiologia 578: 65–77.
Padisák, J., 1992. 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: 217–230.
Padisák, J., E. Soróczki-Pintér & Z. Rezner, 2003. Sinking
properties of some phytoplankton shapes and the
relation of form resistance to morphological diversity
of plankton—an experimental study. Hydrobiologia
500: 243–257.
Putz, J. F., 1995. The golden section and the piano sonatas
of Mozart. Mathematics Magazine 68: 275–282.
Reynolds, C. S., 1997. Vegetation Processes in the Pelagic:
A Model for Ecosystem Theory. Ecology Institute,
Oldendorf/Luhe: 371 pp.
Reynolds, C. S., 2007. Variability in the provision and
function of mucilage in phytoplankton: facultative
responses to the environment. Hydrobiologia 578: 37–
45.
Reynolds, C. S., V. Huszar, C. Kruk, L. Naselli-Flores & S.
Melo, 2002. Towards a functional classification of the
freshwater phytoplankton. Journal of Plankton Research 24: 417–428.
Salmaso, N. & J. Padisák, 2007. Morpho-Functional
Groups and phytoplankton development in two deep
lakes (Lake Garda, Italy and Lake Stechlin, Germany). Hydrobiologia 578: 97–112.
Sommer, U., 1998. Growth and survival strategies of
planktonic diatoms. In Sandgren, C. D. (ed.), Growth
and Reproductive Strategies of Freshwater Phytoplankton: Cambridge University Press, Cambridge,
227–260.
Stoyneva, M. P., J.-P. Descy & W. Vyverman, 2007. Green
algae in Lake Tanganyika: Is morphological variation
a response to seasonal changes? Hydrobiologia 578:
7–16.
Thompson, D. W., 1992. On growth and form. Abridged
edition by J. T. Bonner. Cambridge Univerity Press,
368 pp.
Van Donk, E., 1997. Defenses in phytoplankton against
grazing induced by nutrient limitation, UV-B stress
and infochemicals. Aquatic Ecology 31: 53–58.
123