Winter is considered a dormancy period for phytoplankton, mainly due to the absence of light an to low temperatures. But is it? We have found diverse phytoplankton communities under the ice and their fatty acids reveal they are excellent quality food for zooplankton.
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Phytoplankton communities and their fatty acids in winter
1. Phytoplankton communities and their fatty acids in winter
Pierre Carrier-Corbeil1, Milla Rautio1
1Université du Québec à Chicoutimi, 555 boul. de l’Université G7J2B1 Chicoutimi (Québec) Canada
1Groupe de Recherche Interuniversitaire en Limnologie et en environnement aquatique
Introduction
Most of the world’s lakes show ice formation during their normal
seasonal patterns. Traditionally, lakes have been considered in a state
of idleness during winter and thus, very little research has been
conducted on winter lake dynamics. However, recent observations have
raised awareness to multiple ecological processes occurring in under-
ice lakes. These new observations coincide with an increased societal
understanding of the magnitude and diversity of global warming effects
on ecosystems. Recent studies show that lake and river ice is getting
more scarce as a trend related to global changes. Furthermore, winter
conditions have been shown to influence the ice-free period’s
dynamics. Therefore, in order to augment our understanding of lakes
ecosystemic responses to global changes, it is essential to understand
the unperturbed dynamics of under-ice lakes.4
Phytoplankton is believed to be strongly impacted by the ice cover due
to the important decline in available light for photosynthesis.
Furthermore, phytoplankton are sensitive to the environmental
conditions so changes in winter conditions are expected to drive strong
responses in community dynamics. Since phytoplankton are at the base
of the food web, changes in their biomass, identity and quality are
expected to drive responses in the upper trophic levels. We thus
focussed on winter phytoplankton dynamics in this project.
Objective
Compare winter and summer seston nutritional quality as well as
phytoplankton communities
Hypotheses
• The fatty acid (FA) composition in winter will differ from that of
summer because of expected changes in taxonomy of
phytoplankton.1
• Winter seston will be richer in polyunsaturated fatty acids (PUFA)
and omega 3 because of the homeoviscous response, but will be
deprived of omega 6 because of the lower terrestrial inputs during
that season.1
• Because the environmental conditions are different, summer and
winter phytoplankton communities will have differences in their
compositions.
• The winter communities will be dominated by smaller cells that have
higher surface to volume ratios because they are better able to gather
nutrients and light.
• Diversity, richness and equitability will be lower in winter, compared
with summer, because of the harsh environmental conditions that will
favor only few specialized species.
Methods
We collected phytoplankon samples with a high frequency sampling
from July 2011 to November 2013 in lake Simoncouche (Saguenay,
Quebec, Canada), collecting 17 open water and 10 ice covered
communities for taxonomy and 18 open water and 7 ice covered samples
for FA. We defined summer and winter according to the absence or
presence of ice cover respectively.
Taxonomy and biomass of phytoplankton were evaluated with inverted
microscopy using Utermöhl sedimentation chambers of lugol fixed
samples.
Fatty acids were transmethylated from freeze-dried material using
methanolic HCL and toluene before recuperation in hexane and injection
in a GC-MS system. Quantification was based on an internal standard
(nonadecanoïc acid) and standard curves of known standards.
T tests were used for the univariate data. NMDS were produced for
visual exploration of the data and PERMANOVA and PERMDIST2 tests
were used to confirm the observed patterns in the NMDS.
An indicator species analysis was also performed on phytoplankton
community data to identify species and classes associated with summer
or winter. The analysis is described in Dufrene and Legendre (1997)2 and
selects taxa with highest exclusivity (presence only in one group) and
fidelity (presence in all samples of the group), then uses a permutation
approach to test for significativity of the attributed indicator value.
Results – Phytoplankton Taxonomy
Results – Seston Fatty Acids
Interpretation
Fatty acids did not show any differences between winter and summer except that winter values show
less variance. This is probably due to the harsh conditions restricting the number of available viable
strategies for survival.
Winter and summer phytoplankton communities are different from one another in terms of
taxonomy, biomass, richness and diversity. The lower biomass, richness and diversity indicate that
winter is a strong stressor to the phytoplankton communities. However, these declines were smaller
than expected with 43% of biomass, 68% richness, 80% diversity and 91% equitability remaining in
winter.
The lack of fatty acid changes in presence of taxonomic changes tend to show that the natural effect
of temperature is stronger than the effect of taxonomy for the fatty acid composition of seston.
The results of the indicator species analysis revealed that the typical winter species and classes were
not the expected small organisms. Instead, they are comprised of medium to big cells. The presence
of Dinophyceae and Cryptophyceae suggests that mixotrophy is an important winter adaptation, thus
bigger sizes are advantageous. The fact that diatoms, purely autotrophs, are associated strongly with
summer supports this idea as well.3
Figure 1: Time series of absolute (A) and relative (B) contributions of different FA
groups to total FA content (MUFA = Monounsaturated FA, SAFA = Saturated FA)
Figure 2: Non-metric multidimensional scaling of the FA signatures of
each sampling date based on an euclidean dissimilarity matrix. 2D stress
is 0,15. Ellipses show the distribution of summer and winter values Data
was square root transformed and Wisconsin double standardised.
.
Figure 3: Summer and winter distributions of total FA (A), PUFA (B), Omega
3 (C) and Omega 6 (D) with significance values
Figure 4 :Time series of absolute (A) and relative (B) contributions of phytoplankton
classes to total biomass (CHL = Chlorophyceae, CHR = Chrysophyceae, CON =
Conjugatophyceae, CRY = Cryptophyceae, CYA = Cyanophyceae, DIA = Diatoms,
DIN = Dinophyceae, EUG = Euglenophyceae, RAP = Raphidophyceae, TRE =
Trebouxiophyceae, OTH = Others
Figure 5 : Non-metric multidimensional scaling of the biomass structure of
each sampling date based on a bray-curtis dissimilarity matrix. 2D stress is
0,21. Ellipses show the distribution of summer and winter values. Data
was square root transformed and Wisconsin double standardised.
Figure 6 : Summer and winter distributions of total biomass (A), richness
(B), Shannon’s diversity index (C) and Shannon’s equitability (D) with
significance values
Figure 7 : Seasonal patterns of richness (A), Shannon’s
diversity index (B) and Shannon’s equitability (C)
Table 1 : Indicator value, exclusivity, fidelity and
associated season of different phytoplankton taxa
Conclusions
• Phytoplankton is
abundant, diverse and
specialized under the ice
• Nutritional quality of
seston is the same in
summer than in winter
ReferencesAcknowledgements
Thanks to NSERC for partly funding this project with 3 undergraduate student
research awards. We are grateful for GRIL’s Lac Sentinel project for the
partial funding and logistical help during the second year of sampling. Core
funding was provided by the Canada Research Chair Program.
We would like to thank all members of Laboratoire des Sciences Aquatiques ,
especially Anne-Lise Fortin, Guillaume Grosbois, Sonya Lévesque, Tobias
Schneider, Joannie Venne and Maxime Wauthy for their precious help in all
aspects of this project.
We finally would also like to thank technician Patrick Nadeau for his support
in the field.
• 1Arts, M. T., Brett, M. T., and Kainz, M.: Lipids in aquatic ecosystems, Springer New York, 2009.
• 2Dufrêne, M., and Legendre, P.: Species assemblages and indicator species : The need for a flexible asymmetrical
approach, Ecol. Monogr., 67, 345-366, 1997.
• 3Flynn, K. J., Stoecker, D. K., Mitra, A., Raven, J. A., Glibert, P. M., Hansen, P. J., Granéli, E., and Burkholder, J. M.:
Misuse of the phytoplankton–zooplankton dichotomy: The need to assign organisms as mixotrophs within
plankton functional types, J. Plankton Res., 35, 3-11, 2013.
• 4Hampton, S. E., Galloway, A. W. E., Powers, S. M., Ozersky, T., Woo, K. H., Batt, R. D., Labou, S. G., O'Reilly, C. M.,
Sharma, S., Lottig, N. R., Stanley, E. H., North, R. L., Stockwell, J. D., Adrian, R., Weyhenmeyer, G. A., Arvola, L.,
Baulch, H. M., Bertani, I., Bowman, L. L., Carey, C. C., Catalan, J., Colom-Montero, W., Domine, L. M., Felip, M.,
Granados, I., Gries, C., Grossart, H.-P., Haberman, J., Haldna, M., Hayden, B., Higgins, S. N., Jolley, J. C., Kahilainen,
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S. B., Whiteford, E. J., and Xenopoulos, M. A.: Ecology under lake ice, Ecol. Lett., 20, 98-111, 2017.
Taxon Season Indicator
Value
Exclusivity Fidelity p
value
Asterionella Summer 0.886 0.8628 0.9091 0.040
Synedra Summer 0.863 0.9100 0.8182 0.010
Anabaena Summer 0.852 0.9399 0.7727 0.005
Elakatothrix Summer 0.712 0.9290 0.5455 0.030
Oocystis Summer 0.707 0.9984 0.5000 0.020
Tetraëdriella Summer 0.603 1.0000 0.3636 0.050
Rhodomonas Winter 0.742 0.7945 0.6923 0.035
Peridinium Winter 0.696 0.8992 0.5385 0.035
Klebsormidiophyceae Summer 0.712 0.9290 0.5455 0.015
Dinophyceae Winter 0.734 0.7784 0.6923 0.025