13
Long-Term UVR Effects Upon
Phytoplankton Natural Communities
of Patagonian Coastal Waters
Silvana R. Halac1,2, Virginia E. Villafañe1,3,
Rodrigo J. Gonçalves1,3 and E. Walter Helbling1,3
1Estación
de Fotobiología Playa Unión (EFPU), Chubut,
2Instituto Nacional del Agua (INA), Córdoba,
3Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET),
Argentina
1. Introduction
Since the discovery of the ozone “hole” over the Antarctic continent and the concomitant
increase in ultraviolet B radiation (UV-B, 280-315 nm) vast literature has been produced
about the impact of these wavelengths on aquatic organisms. Nowadays it is widely
accepted that ultraviolet radiation (UVR, 280-400 nm) acts as a stressor for both organisms
and ecosystems, this being true not only for increased UVR but also for ‘normal’ levels (see
review by Helbling and Zagarese 2003 and references therein). Many studies about the UVR
impact on phytoplankton species and communities have reported negative effects on
different cellular targets (e.g., photosystem II, DNA, proteins) which may affect several
processes such as growth and photosynthesis (Vernet 2000; Villafañe et al. 2003). In
particular, it has been found that UVR can significantly affect Photosynthesis versus
Irradiance (P vs. E) parameters (Furgal and Smith 1997; Montecino et al. 2001; Villafañe et al.
2004c) thus remote sensing calculations of primary production based on them might be
frequently overestimated.
On the other hand, some studies also documented positive effects of UVR, such as increased
carbon uptake under UV-A (315-400 nm) exposure (Nilawati et al. 1997, Barbieri et al. 2002;
Helbling et al. 2003). Exposure to UV-A can also induce the light-dependant enzymatic
repair of the UVR-induced DNA damage (i.e., ‘photorepair’, Buma et al. 2003). Indirect
effects of UVR such as the breakdown (photolysis / photodegradation) of dissolved organic
matter (DOM) (Osburn and Morris 2003) can be either beneficial for organisms by means of
increasing nutrient availability, or detrimental, by increasing water transparency so cells
receive more irradiance (Cooke et al. 2006). It is also known that the interaction of UVR and
other factors – e.g., nutrient availability, vertical mixing, changes in temperature,
supersaturating oxygen concentrations or high pH values, may strongly condition the
observed results (Forster and Schubert 2001; Neale et al. 2003; Beardall et al. 2009 and
references therein) as compared to those obtained considering only UVR. This is due to the
synergic or antagonistic nature of the interactions between UVR and those other factors
(Dunne 2010). The evaluation of the combined effects of increased temperature and UVR is
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particularly interesting because these two variables are more affected in a global change
scenario (Häder et al. 2011). In this regard, some studies have demonstrated that increased
temperature under UVR exposure benefits photosynthetic performance of some diatoms
species by enhancing repair rates (Sobrino and Neale 2007; Halac et al. 2010); however, in
studies carried out with cyanobacteria, Fiorda Giordanino et al. (2011) found important
inter-specific variability in responses (with some species benefiting from increased
temperature whereas others were rather indifferent) and these variations were partially
related to differences in morphology among the species.
In spite of the negative effects, there are several mechanisms that allow phytoplankton to
cope with UVR over time periods of days / weeks: At the individual level, the most
common strategy is the synthesis of protective compounds such as mycosporine-like amino
acids – MAAs. As the maximum absorption of these compounds lies between 310 and 360
nm, they have the potential of decreasing the energy of the most damaging portions of the
solar spectrum (Banaszak 2003; Korbee et al. 2006). Pigments like carotenoids can also
protect organisms by dissipating excessive energy as heat i.e., via non-photochemical
quenching (Müller et al. 2001). Another common protective strategy for motile organisms is
to avoid UVR by performing downward migration (Richter et al. 2007). Finally, some
organisms have the ability to repair damage produced to the DNA molecule (Buma et al.
2003) or photosystem components, especially the D1 protein (Andersson and Barber 1996;
Halac et al. 2009). All together, the net impact of UVR is the result of a trade-off between the
sensitivity of individual / community and their acclimation capacity.
2. Assessment of UVR effects upon phytoplankton over long-term periods
Although extensive research has been carried out to address the short-term effects of UVR
on phytoplankton (i.e., with experiments lasting less than one day, see review by Villafañe
et al. 2003) the performance of communities over longer temporal scales (i.e., days / weeks)
have been relatively less studied. Still, these studies are especially important because they
reflect the result of a particular effect caused by UVR as well as potential photoacclimation
i.e., short-term experiments frequently overestimate the impact of UVR. One way to
evaluate UVR effects on aquatic autotrophic organisms on a long–term basis is by using an
“enclosed ecosystem” as a model (named meso- or microcosms, depending on the volume
of sample) in which a water parcel is isolated and incubated under conditions similar to
those found in the natural environment (Wängberg et al. 1996). These setups make feasible
to conduct controlled incubations of plankton communities while allowing the manipulation
of UVR intensities (i.e., when working with artificial radiation sources) and spectral
composition (by covering the containers with different filters / materials). On the other
hand, natural conditions are not completely simulated in these cases, as for example water
movements are restricted and larger organisms are usually excluded. In these experiments
phytoplankton biomass tends to increase rapidly therefore, they often reproduce blooms
conditions (Belzile et al. 2006 and references therein).
Studies devoted to evaluate the effects of UVR on phytoplankton communities over long
periods of time have highlighted the high variability in responses. Some outdoor
mesocosms studies showed little UVR effects on chlorophyll a (Chl a) content (Halac et al.
1997; Wängberg et al. 1999; Whitehead et al. 2000). On the other hand, Forster et al. (2001)
working with phytoplankton of the Darss-Zingst estuary in the Baltic Sea found higher Chl a
concentration in samples that did not receive UVR, as also observed in the experiments
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231
carried out by Keller et al. (1997) with communities off Narragansett Bay. At the community
level, UVR impact is frequently translated onto changes in the taxonomic composition
towards more tolerant species or changes in size distribution. For example, studies carried
out by Wängberg et al. (1999; 2008) found that small phytoplankton were favored by UV-B
exposure, and Mousseau et al. (2000) reported a shift from diatoms to small naked
flagellates that occurred more rapidly under enhanced UV-B than under its natural levels.
UVR-mediated community structure shifts may result in an important impact for the whole
aquatic system, either by altering the food web structure due to the differential sensitivity to
UVR, or by affecting carbon allocation into different biomolecules which in turn is
translated into changes of carbon and nutrient cycling in the ecosystem (Mostajir et al. 1999;
Sommaruga 2003).
3. Why studying UVR effects upon phytoplankton communities of Patagonia?
The ecological effects of UVR were documented more intensively in the Antarctic region at
beginning of the awareness of the Antarctic ozone ‘hole’. Later studies pointed out that the
influence of the Antarctic ozone depletion extends to mid latitudes (Atkinson et al. 1989)
and that Southern mid latitudes may be even more affected (Seckmeyer and McKenzie
1992). Still, while many studies about the effects and impact of UVR on phytoplankton have
been carried out in polar areas, relatively less is known about temperate regions (see review
by Gonçalves et al. 2010) such as Patagonia. The Patagonia region is located at the southern
tip of South America, includes part of Argentina and Chile (Fig. 1) and has unique
characteristics that would warrant UVR studies for several reasons. First, the area is
occasionally under the influence of ozone-depleted air masses from the Antarctic polar
vortex, thus experiencing periods of enhanced UV-B (Villafañe et al. 2001; Helbling et al.
2005). Second, its great variability in cloudiness, from high cover over the Andes and subAntarctic regions to the relatively clear skies on the mid-latitude Atlantic coast, creates a
range of environments with variable UVR climatology. Third, it presents a high variability
in the nature and bio-optical characteristics of its water bodies (e.g. the upwelling deep
waters in the Pacific and the shallow and very productive Atlantic waters). Finally, high
wind speed and frequency, especially during spring and summer (Villafañe et al. 2004a;
Helbling et al. 2005) strongly condition the depth of the upper mixed layer (UML) and hence
the underwater radiation field to which organisms are exposed. In addition the assessment
of the UVR impact on phytoplankton from Argentinean Patagonia is essential since these
organisms are responsible for an important share of primary productivity in the
Argentinean Sea (Lutz et al. 2010) and they constitute the base of a very rich food web that
includes fishes (e.g. hake, anchovy) (Skewgar et al. 2007) and invertebrate species (e.g.
shrimp and mussels) of great commercial value (Caille et al. 1997).
Taking into consideration these facts, in the next section we present our study case and a
review of the current knowledge about UVR effects on phytoplankton communities mainly
from Patagonia, and especially focusing on effects observed in a days/weeks timeframe.
4. Study case: Long-term UVR effects on phytoplankton from Bahía Engaño,
Patagonia, Argentina
The study site (Bahía Engaño, Chubut, Argentina) is located at Northern coastal Patagonia
(Fig. 1). Our research group had previously conducted several UVR studies with
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Fig. 1. Location of the study site, showing Patagonia (shaded area) and the relative position
of the Chubut Province (Argentina) in South America. The inset shows the study area where
microcosms experiments were done.
phytoplankton communities from this area, mostly determining short-term responses,
particularly those related to inhibition of carbon fixation and photoinhibition (e.g., see
Barbieri et al. 2002; Villafañe et al. 2004a; Villafañe et al. 2004b; Villafañe et al. 2008; Helbling
et al. 2010), and relatively less studies to determine long-term responses to UVR in
combination with nutrient addition (Helbling et al. 2005, Marcoval et al. 2008). Therefore,
the results presented here aim to further elucidate aspects of UVR sensitivity and
photoacclimation of phytoplankton from Patagonia occurring over longer periods of time,
especially focusing on community properties such as global growth, abundance, taxonomic
composition and size distribution.
An experimental approach was taken, in which natural phytoplankton samples were
collected, and incubated under solar radiation during the austral summer of 2010. The
experiments consisted in two microcosm incubations (hereafter MI and MII) which lasted
between February 5 - 11 (MI) and February 15 - 21 (MII). The experimental setup consisted
in exposing natural phytoplankton samples in 25-l, UVR-transparent bags (microcosms)
under three different radiation conditions: a) PAB, 280-700 nm (samples receiving PAR+UVA+UV-B); b) PA, 320-700 nm (samples receiving PAR+UV-A) and c) P, 400-700 nm (samples
receiving only PAR). The microcosms (duplicates per radiation treatment) were placed in a
Long-Term UVR Effects Upon Phytoplankton
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tank (3 m diameter, 1 m depth) with running water as temperature control and exposed to
solar radiation at the surface for ca. 7 days. During the experiments, water samples from
each microcosm bag was collected daily (early in the morning) for analyses of Chl a and UVabsorbing compounds whereas samples for taxonomic composition and size distribution
were taken every other day.
During the experiments, PAR and UVR irradiance conditions (Fig. 2) presented a typical
pattern of relatively high values at noon and low ones during the morning and late
Fig. 2. Solar radiation reaching the Earth’s surface at the study site during experiments
carried out during February 5-11 (Julian days 36-42) (MI), and February 15-21 (Julian days
46-52), 2010 (MII). Irradiance is shown for: A) PAR, 400– 700 nm, B) UV-A, 315–400 nm and,
C) UV-B, 280-315 nm. Solar radiation was continuously monitored using a broad-band filter
radiometer (ELDONET, Real Time Computers, Möhrendorf, Germany, Häder et al. 2007)
permanently installed on the roof of the Estación de Fotobiología Playa Unión.
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afternoon; also, the presence of clouds that resulted in high daily variability in solar
irradiance is characteristic for the area during summer (Helbling et al. 2005). During our
experiments, maximum PAR irradiance levels were rather similar (~440 – 460 W m-2) (Fig.
2A) as also were UV-A (~60 W m-2) and UV-B (~2 W m-2) – except for the second day during
MII where PAR and UVR values were very low (i.e., ~100, 17, and 0.6 W m-2 for PAR, UV-A
and UV-B, respectively; Figs. 2A-C). The high irradiance values in combination with long
daylight periods result in high daily doses (Helbling et al. 2005) which are similar to those
registered in tropical environments (Gao et al. 2007). Since phytoplankton in our
experiments were exposed to these high irradiance conditions of solar radiation under a thin
layer of water under, our results represent the ‘worst-case scenario’, i.e., as if cells were at
the water surface, not allowed to move downward towards lower radiation levels.
Because the timing of our sampling (summer) that is considered a post-bloom condition for
our study area (Villafañe et al. 2008), we added nutrients to each incubation bag (f/2
concentration (Guillard and Ryther 1962)) at the beginning of each experiment to avoid
nutrient constraints while phytoplankton was growing. In both experiments, the
phytoplankton assemblage showed an increase, as assessed by measurements of Chl a (Fig.
3A), cellular abundance (Fig. 3B) and autotrophic carbon (Fig. 3C). Some general features
were observed: Firstly, during both experiments the variables used to calculate growth had
a typical exponential increase, similar to those occurring at bloom conditions, and thus an
optimum cellular response. Secondly, the observed increase was similar for both
experiments, although some differences appeared for some variables; and thirdly, no
general UVR effects were observed (except in a few cases) within any experiment / variable
measured.
As an overview of the increase of phytoplankton assemblages, Table 1 resumes the
calculated growth rates (µ) during both experiments. The fast growth observed during the
experiments were probably due to the addition of nutrients and the low turbulence inside
the incubation bags, as previously observed in long-term studies with phytoplankton
communities from the area (Helbling et al. 2005; Marcoval et al. 2008). As mentioned before,
a common result of long-term incubations is the lack of UVR effects on growth and biomass,
as also observed in our study (i.e., no-significant differences between radiation treatments as
observed in Table 1 and Fig. 3). In fact, this lack of UVR effects on growth was also observed
in other studies carried out in Patagonian waters: For example, Roy et al. (2006) working
with phytoplankton communities from the Beagle Channel (Tierra del Fuego) observed
minor changes in biomass due to UV-B (both normal and enhanced levels), even though the
UV-B enhancement imposed to the samples was important (i.e., simulating 60 % of ozone
depletion). However, Hernando et al. (2006) found a significant effect of UVR on growth on
these phytoplankton assemblages only when samples were exposed to solar radiation at
fixed depths, in contrast to the mixed conditions imposed in the mesocosms described by
Roy et al. (2006). In addition, Helbling et al. (2005) and Marcoval et al. (2008) determined
variable UVR-induced inhibition of growth in natural communities off the Chubut coast
under different conditions of nutrients availability, with nutrient-depleted samples being
more sensitive to UVR than those in which nutrients had been added. Therefore, UVR alone
is not an evident inhibitor of growth for phytoplankton off Patagonia waters, but it can have
important effects when acting together with other stressors (e.g., nutrient availability,
mixing conditions).
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Fig. 3. Growth of the phytoplankton communities during MI and MII experiments evaluated
as: A) Chlorophyll a (Chl a) content (measured by fluorometric and spectrophotometric
techniques, Holm-Hansen and Riemann 1978; Porra 2002); B) Cell concentration (obtained
by microscopy; Villafañe and Reid 1995); and C) Autotrophic biomass (considering
biovolumes according to Hillebrand et al. 1999 and posterior transformation to carbon
content following Strathmann 1967). The different radiation treatments are shown in
different colors. The vertical lines on the symbols indicate the half mean range. Note the
different log scales for the variables presented.
Another observed pattern in the growth response was, at first sight, a similar trend among
experiments which was due not only to the similar radiation conditions (Fig. 2) but also to
the initial assemblages used in both experiments (i.e., similar starting taxonomic
composition). In fact, at the beginning of experiments, the communities were numerically
dominated by flagellates (e.g., chlorophytes and cryptophytes) and to a less extent by
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Growth rates (µ; d-1)
Chl a
Cellular abundance
Autotrophic carbon
PAB
P
PAB
P
PAB
P
Microcosm
I
0.76 ± 0.01
0.76 ± 0.06
0.88 ± 0.09
0.79 ± 0.04
0.84 ± 0.14
0.75 ± 0.15
Microcosm
II
0.94 ± 0.02
0.90 ± 0.03
0.73 ± 0.08
0.73 ± 0.11
0.70 ± 0.07
0.76 ± 0.03
Table 1. Growth rates (µ, in d-1) during MI and MII experiments, determined from
measurements of Chl a, cellular abundance and estimations of autotrophic carbon.
diatoms (Thalassiosira spp., Nitzschia longissima); on the other hand, the abundance of
dinoflagellates (e.g., Prorocentrum micans, unidentified naked species) was very low. This is
in agreement with previous studies carried out in the area that demonstrated the
conspicuous presence of flagellates during the summer (Villafañe et al. 2004a; Villafañe et al.
2008). However, it was also evident that there were some differences in the growth rates
calculated from different variables as well as when comparing experiments. For example,
during MI, Chl a-based µ were lower than those from cellular abundance and autotrophic
carbon, while the opposite occurred in MII. The fact that Chl a concentration showed a
slower (during MI) or faster (during MII) increase than the other two variables, suggests a
differential acclimation of the assemblages as the experiments progressed. This could be due
to different reasons: On the one hand, as the community grew the self-shading effect might
become important and thus the Chl a concentration per cell would increase to keep
efficiently capturing photons and maintain the exponential growth. This could be mediated
by cell size, as smaller cells (i.e., higher surface-to-volume ratio) needs comparatively less
Chl a per cell as compared to larger cells (Falkowski 1981). On the other hand, an increase in
cell size, with larger cells towards the end of the exponential growth phase, means a smaller
surface-to-volume ratio and thus the need of higher Chl a content per cell. Indeed, a
combination of both factors were observed in our experiments, as the C to Chl a ratio – an
indicator of “light acclimation” - increased in MI and decreased in MII, while the Chl a
content per cell decreased in MI and increased in MII towards the end of the exponential
phase (Table 2). In the following paragraphs we will discuss how changes in cell size,
together with differential changes in species composition might have accounted for the
observed patterns and variability among our experiments.
C / Chl a
Chl a content per cell
PAB
P
PAB
P
MI - T0
35 ± 5
35 ± 5
1.87 ± 0.45
1.87 ± 0.45
MI - Tf
58.8 ± 3.1
33.2
0.88 ± 0.33
1.48
MII - T0
94.6 ± 0.9
94.6 ± 0.9
0.65 ± 0.18
0.65 ± 0.18
MII - Tf
37 ± 13
53.8 ± 15.7
1.49 ± 0.07
1.33 ± 0.02
Table 2. Mean (and half mean range) carbon to Chl a ratio (in µg C µg Chl a-1) and Chl a
content per cell (in pg) at the beginning (T0) and at the end (Tf) of the experiments.
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To study changes in the size spectra of each treatment, we recorded digital images of each
sample and analyzed them to obtain the size (area) distribution of cells at the beginning of
the incubation as well as at the end of the exponential growth. The size spectra data (Fig. 4)
indicates that in both experiments most of the phytoplankton assemblages (> 60 %) were
dominated by small cells with an area < 100 µm2 (Figs. 4A and C). A shift in the cumulative
frequency of cell size in the range of 65-395 µm2 was observed in all radiation treatments of
MI (Fig 4B), being the P treatment the one with the higher change. On the other hand,
during MII (Fig 4D) a slightly different response was observed, as the P treatment showed
virtually no changes but the size distribution in the PAB treatment was slightly shifted
towards larger areas in the range 85-395 µm2. It has been usually found in other studies that
smaller cells tend to dominate the community after UVR-exposure (Mostajir et al. 1999), but
in our results this might be strongly affected by the initial conditions of each microcosm.
Also we can not rule out the effects of co-occurring predators (i.e., heterotrophic
microplankton). Similarly to what we expressed about the lack of UVR-only effects on
growth, we could speculate that UVR alone might not always show evident effects on size
distribution, but depending on the starting taxonomic composition of the community, both
PAR and UVR may have implications in the structure of the plankton community.
Fig. 4. Cumulative frequency of size (in µm2) at the beginning (T0) and at the end of the
exponential growth phase for MI (A) MII (C). In B) and C) a detailed view within the size
ranges of differences is shown. The radiation treatments are shown in different colors: P
(green), and PAB (red). Size distribution was evaluated in formalin-fixed samples from
pictures taken under an inverted microscope; images were analyzed using Image J software
(Abramoff et al. 2004).
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Microscopical analyses of the communities also supported changes in cell size throughout
the experiments. For example, carbon allocated in the nanoplankton fraction (cells < 20 µm
in effective diameter) increased more rapidly than that of microplankton (> 20 µm) in MI
(Fig. 5A), but the opposite occurred in MII (Fig. 5 B). Also, there was a general decrease in
the microplankton biomass from T0 towards the end of the experiments (Fig 5C) as was also
expected from the shift towards smaller cells in MI (Fig 4B). However, the decrease was more
pronounced in MI than in MII, therefore the overall result was that the relative contribution of
microplankton to the total biomass in MII was higher than during MI (Fig 5C).
Fig. 5. Autotrophic carbon (in μg C l-1) of the phytoplankton size classes: A) Nanoplankton
(<20 µm) and, B) Microplankton (≥20 µm). C) Relative contribution of nanoplankton and
microplankton (%) to the total autotrophic carbon at the beginning (T0) and at the end of the
MI and MII experiments. The radiation treatments / size fractions are shown in different
colors: P (green) and PAB (red) / microplankton (green) and nanoplankton (orange). The
vertical lines on the symbols indicate the half mean range.
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Any change in cell size and biomass allocation might occur within a particular species
however they normally are associated to change in taxonomic composition towards the
most resistant or acclimated groups. In fact, the most evident effect of UVR exposure (as
compared to samples in which UVR was excluded) over long periods of time are the
taxonomic changes produced in the community, which act as a photoacclimation
mechanism. There are many studies that have reported this effect in long-term experiments
(see review by Villafañe et al. 2003) but in particular, and for the Patagonia area, Hernando
et al. (2006) working with the communities off the Beagle Channel observed changes from
an assemblage co-dominated by phytoflagellates and diatoms at the beginning of the
experiments to a progressive increase of euglenophytes, especially under static conditions of
Fig. 6. Autotrophic carbon (in μg C l-1) of: A) Diatoms, B): Flagellates and, C) Dinoflagellates
during the experiments MI and MII. The radiation treatments are shown in different colors:
P (green), and PAB (red); different lines in panel A indicate the contribution to the total of
centric (solid lines) and of pennate diatoms (dotted lines). The vertical lines on the symbols
indicate the half mean range.
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the water column. In studies carried out with communities off the Chubut coast, Helbling et
al. (2005) and Marcoval et al. (2008) also found that solar radiation played a fundamental
role in shaping phytoplankton communities. In order to further explore these changes in
species composition in our experiments, in Fig. 6 we show the contribution of the three main
taxonomic groups - diatoms (centric and pennates), flagellates and dinoflagellates.
Overall, no UVR effects were observed in the diatoms in both experiments (Fig. 6A) while
significant differences among radiation treatments became evident in flagellates (Fig. 6B)
and in dinoflagellates (Fig. 6C). For example, autotrophic carbon in flagellates was
negatively affected by UVR, resulting in significantly lower values in samples receiving
UVR (PAB treatment) as compared to those that received only PAR (P treatment). On the
contrary, autotrophic carbon in dinoflagellates was higher in samples receiving UVR.
Previous studies (Hernando and San Román 1999; Hernando et al. 2005) have shown similar
results about the sensitivity of flagellates. In the case of dinoflagellates, their response seems
to be more related to the size as shown by Helbling et al. (2008) where larger species (i.e.,
Prorocentrum micans, 50 μm mean diameter) were less sensitive than small ones such as
Gymnodinium chlorophorum (5 μm) and Heterocapsa triquetra (20 μm).
However, the overall picture in our experiments shows a significantly higher increase of
autotrophic carbon in diatoms (both centric and pennates) (Fig. 6A) with centric diatoms
always accounting for the higher share at the end of the experiments, as compared to
flagellates (Fig. 6B) and dinoflagellates (Fig. 6C). This differential increase in autotrophic
carbon caused a shift in the community dominance from a flagellate-dominated community
towards a diatom-dominated one (Fig. 7).
Fig. 7. Autotrophic carbon in diatoms, flagellates and dinoflagellates during the MI and MII
experiments. The radiation treatments are shown in different colors: P (green), and PAB
(red); filled lines: diatoms, dotted lines with squares: flagellates and dotted lines with
diamonds: dinoflagellates. The vertical lines on the symbols indicate the half mean range.
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It should be noted that at the beginning of the experiments, the contribution of diatoms to
the total abundance and biomass was very small (Figs. 6 and 7) and they were represented
by Thalassiosira spp., Niztschia longissima, Skeletonema costatum, Asterionellopsis glacialis and
unidentified pennates, among some others. However, by the end of the experiment, centric
diatoms accounted for ca. 75% and 66% of the total autotrophic carbon for MI and MII,
respectively. By the end of MI, and in both radiation treatments Thalassiossira spp. with a
size range of 10-20 µm almost completely dominated the assemblages (Fig. 8). On the other
hand, in MII there was a co- dominance of Thalassiossira spp. of 10-20 µm size and larger
ones (> 20 µm).
Fig. 8. Relative contribution of diatoms to the total autotrophic carbon at the beginning (T0)
and at the end of experiments. The size classes of Thalassiosira (Th.) are shown in different
colors: > 20 µm (yellow), 10-20 µm (red); other diatoms are represented in green.
So far, two main outcomes can be suggested from our data, one is related to changes in cell
size (and consequently those on biomass, Chl a content per cell, etc.) and the other is that in
species composition towards a diatom-dominated (mainly centric) assemblages. Although
these are important acclimation mechanisms occurring over longer periods of time, there are
also alternative ones to cope with UVR and excess of irradiance. One of such mechanism is,
as previously mentioned, the synthesis of UV-absorbing compounds (mainly mycosporine
like amino acids, MAAs). It has been found that even MAAs are generally very low in
natural communities of Patagonia (Barbieri et al. 2002; Villafañe et al. 2004a; Villafañe et al.
2004c; Marcoval et al. 2008) but some species i.e., dinoflagellates such as Prorocentrum micans
are able to synthesize them in high amounts after prolonged UVR exposure (Marcoval et al.
2007; Helbling et al. 2008); diatoms are also known to produce relatively high amounts
(Lagunas et al., unpubl. data). It has also been shown that the synthesis of UV-absorbing
compounds is more effective in large cells whereas in small species their synthesis would be
too costly and osmotically disadvantageous (Garcia-Pichel 1994). In addition, previous
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studies (Helbling et al. 1996) showed that centric diatoms were able to synthesize significant
amounts of UV-absorbing compounds after long-term exposure to UVR, whereas pennates
did not. In our study case it is interesting to note that no significant changes in the
concentration of UV-absorbing compounds were observed during MI (data not shown)
probably due to the dominance of small diatom species during the experiment (Fig. 8). On
the contrary, during MII there was a significant increase of UV-absorbing compounds (Fig
9). This increase, relative to the Chl a content, was significant (Fig 9B) but there were no
differences among radiation treatments, suggesting that all wavelengths of solar radiation
triggered the synthesis of these compounds, as also observed for Antarctic diatoms
(Helbling et al. 1996). A possible explanation is that high solar radiation in their natural
environment will include PAR and UVR, therefore PAR as well as UVR may be capable of
triggering the synthesis of MAAs so Thalassiossira spp. can obtain protection against solar
UVR (Helbling et al. 1996). The presence of UV-absorbing compounds in MII probably
reflects the higher proportion of large Thalassiossira species during this experiment (Fig 8)
and also of dinoflagellates, although in lesser extent (Fig 6 C).
Fig. 9. A) Absorption spectra at the beginning (T0) and at the end of the MII experiment: B)
UV-absorbing compounds relative to Chl a content (OD337 per µg Chl a-1) throughout the
experiment. UV-absorbing compounds were estimated as described in Dunlap et al. (1995)
using the peak height at 337 nm. The radiation treatments are shown in different colors: P
(green), PA (blue) and PAB (red); dotted lines represent T0.
Long-Term UVR Effects Upon Phytoplankton
Natural Communities of Patagonian Coastal Waters
243
5. Ecological implications
All together, this study indicates that within the experimental time frame, UVR effects are
more evident in the taxonomic composition of the community than on algal growth /
biomass. As stated above, the “starting point” of the studied community was very important
in our incubations, therefore stressing the role of combined factors and preventing simple
extrapolations. Also it suggests that it is not possible to generalize the solar radiation effects
on diverse phytoplankton assemblages: Other factors such as previous light history,
gradients of temperature and nutrient availability, in turn related to water turbulence and /
or UML depth are very important to understand the observed responses. For example, even
when both microcosms showed a sustained growth during several days, the final
distribution of the autotrophic carbon was very different in each case. This may have
important consequences for the available energy sources in the pelagic food web, as species
and size distribution are two of the main factors affecting the chances of a phytoplankton
cell being ingested by a predator. A community with a different carbon source will function
and respond in a different way when exposed to UVR and other factors. It may be difficult
to evaluate these scenarios with Chl a estimations obtained from remote sensing techniques,
but additional in-situ research in this topic would help us to validate those estimations
which proved to be useful for regional-global comparisons.
6. Acknowledgments
We thank V. Fiorda and E. Heimsch for their help during experiments. We are also grateful
with personnel at Estación Marítima Comersonii at Puerto Rawson for sampling collection
for our experiments. This work was supported by Agencia Nacional de Promoción
Científica y Tecnológica (PICT2007-01651, Argentina), Consejo Nacional de Investigaciones
Científicas y Técnicas (CONICET, Argentina) – Deutsche Forschungsgemeinschaft (DFG,
Germany) (CONICET-DFG-2009), Ministerio de Ciencia, Tecnología e Innovación
Productiva (MINCyT, Argentina) – Consejo Nacional de Ciencia y Tecnología (CONACYT,
Mexico) (Project N° MX/09/13) and Fundación Playa Unión. This work is in partial
fulfillment of the Ph.D. thesis of SRH, supported by a scholarship from Agencia Nacional de
Ciencia and Instituto Nacional del Agua (Argentina). This is Contribution N° 124 of Estación
de Fotobiología Playa Unión.
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