The Role of Solar UV on the Development of Macroalgal Assemblages of Greece

The Role of Solar UV on the Development of Macroalgal Assemblages of Greece

R. Santas¹, D. Danielidis², K. Koussoulaki¹, M. Prost³, Ph. Santas¹, and D.-P. Häder³

³^{3

1

1OikoTechnics, Kefallenias 50, A. Helioupolis, GR-16342; e-mail: santas@hol.gr

^{2University of Athens, Dept. Biology, Sect. Ecology and Systematics, Athens,
Greece
^{3Friedrich-Alexander Universität, Staudtsr. 5, Erlangen, Germany

Key words

Algae, mycosporines, standing crop, community analysis, UV-A, UV-B

Abstract

The role of incident PAR, UV-A and UV-B radiation was investigated in macroalgal
assemblages grown in partial enclosures in a natural marine habitat. While
seasonal changes in community structure were observed, the effects of light treatment on
both community structure and standing crop were unclear. During the 12 month experimental period, monthly doses above surface
varied by a factor of 6.4, 7.9, and 12.9 respectively. Exposure to
UV radiation increased the mycosporine content of the assemblages. UV protection provided
by these screening pigments along with the wide natural variations in light doses and
spectral composition are likely explanations for the absence of inhibitory UV effects.

Introduction

The increase in solar ultraviolet radiation due to stratospheric ozone depletion^1,2,3
has raised much scientific and public concern during the last years. UV radiation affects
the biology of living organisms and, therefore, the balance of natural ecosystems. Most
terrestrial and aquatic plant organisms are unable to avoid direct exposure to sunlight.
Benthic algae can be especially susceptible to ultraviolet radiation⁴ as they
lack the protective tissue layers and UV absorbing pigments present in higher plants.
Ultraviolet radiation inhibits the growth of many marine primary producers including
benthic and planktonic microalgae⁵, green algae⁶and several shallow
and deep water species of red algae^6,7. UV has been shown to damage the
photosynthetic systems of green algae^8,9. However, the presence of UV-screening
mycosporine-like amino acids (MAAs) has been reported in certain macroalgal species¹⁰.
Mycosporines show an absorption maximum around 335 nm and have been also found in other
marine organisms¹¹. MAA protection against the damaging effect of short
wavelength radiation has been demonstrated in a wide variety of plants¹².

Enhanced simulated ultraviolet radiation affects microalgal community structure^13,14. The present study was carried out to
investigate the role of ambient ultraviolet radiation on the productivity and structure of
naturally grown macroalgal assemblages. Furthermore, mycosporine production in relation to
light exposure is discussed.

Methods and Materials

Experiments were conducted at a distance of 50m from an east-facing rocky shore of
Saronikos Gulf, near Korinthos, Greece (37^o 58? N, 23^o 0?E). Ceramic tiles (10x10cm) were used as a substrate for algal
attachment and growth. The ceramic tiles were placed in partial enclosures which allowed
for free current flow over the developing algal mats (for a picture of the experimental
apparatus see Reizopoulou et al.¹⁵). The enclosures were suspended from PVC
rafts at 0.5, 1.0 and 1.5 meters for periods of 9,10 and 12 months. Using UV-transmitting
Plexiglas (GS 2458) and plastic foil cutoff filters (295 Ultraphan; PR Montagefolie 320nm
Art. Nr. 10155 099; and 395 Ultraphan UV Opak; thickness: 0.3mm) 3 light regimes were
established (PAR, PAR+UV-A, PAR+UV-A+UV-B). A total of 9 treatments combinations (light
regimes x 3 depths) were performed in duplicate. The filters were cleaned regularly every
two days to prevent alteration of the transmittance properties due to fouling.

On March 16, April 18 and June 25, 1996, i.e. after 9, 10 and 12 months of growth one
ceramic tiles was removed at random from the designated treatment combinations. The entire
growth from each tile was used for algae identification^16,17,18,19 and
enumeration. Subsequently the biomass was collected on fiberglass filters, rinsed with
deionized water, and allowed to dry to constant weight at 80^o C. The biomass data were
subjected to analysis of variance. Multivariate community analysis was performed with the
Primer software (Plymouth Marine Laboratory).

At the end of the experiment (12 months), pigments were extracted in methanol to assess
mycosporine production at the community level.

Results

Light doses

The natural levels of solar incidence above surface varied dramatically during the one
year growth period (fig. 1). The maximum monthly dose for PAR (August 1995; 302,051 kJ m^-2)
was 6.4 times higher than the winter minimum (December 1995; 47,397 kJ m^-2).
The differences in the UV-A and UV-B doses were even sharper. The August/December ratios
for these two bands were 7.9 and 12.9 respectively.

Figure 1: Monthly doses of PAR, UV-A and UV-B as measured with an ELDONET light
dosimeter above surface. UV-A values multiplied by a factor of 10.

Biomass data

Average biomass values for all three sampling events are listed in Table 1.

Table 1: Standing crop (g m^-2)

Treatments
16/3/1996
18/4/1996
25/6/1996

March
April
June

PAR+UVA +UVB 0.5m
353.9
433.3
232.3

PAR+UVA +UVB 1.0m
355.8
241.2
231.9

PAR+UVA +UVB 1.5m
342.7
222.8
214.6

PAR+UVA 0.5m
429.5
378.4
258.9

PAR+UVA 1.0m
225.2
233.2
286.4

PAR+UVA 1.5m
257.0
361.9
255.9

PAR 0.5m
447.7
309.9
240.7

PAR 1.0m
343.5
156.6
170.7

PAR 1.5m
259.0
106.4
197.8

A two-way ANOVA (month vs. light-depth treatment combination) revealed that a) in
April, the biomass of the PAR+UV-A+UV-B at 0.5 m was significantly higher than the PAR
treatments at both 1.0 and 1.5 m, b) in March and June no significant differences in
biomass between the nine light - depth treatment combinations unlike April when the PAR
treatment at 1.5 m was significantly lower than PAR+UV-A at 0.5 and 1.5 m and
PAR+UV-A+UV-B at 0.5 m, and c) within light-depth combinations no significant differences
were observed among the three months (Fig. 2).

Figure 2: Average biomass under the 9 treatment combinations. Error bars: 95%
confidence intervals. Non-overlapping error bars indicate significant differences.

Community analysis

During the first months of substrate colonization the assemblages were dominated by
diatom species. These results are presented elsewhere¹⁵. The structure of the assemblages gradually changed with the appearance of
filamentous macroalgal species. Community development was slower during the winter months.
After the end of the cold season a dense mat of macroalgae formed on the ceramic tiles.
The macroalgal assemblages comprised a total of 60 species of red, green and brown algae.
Species found in all sample events are listed in Table 2. The group with the greatest
number of representative taxa was Rhodophyceae with a total of 41 species, followed by
Chlorophyceae (10 species) and Phaeophyceae (9 species). The largest number of species (8)
within a genus was recorded for the red alga Ceramium.

General remarks: Tables 3-5 list the semiquantitative abundances of the 12 most
common algae. The number of species present under all light treatments (and most depths)
increased from 5 (March) to 8 (April) to 10 (June). Laurencia was present only at
0.5 m, always under PAR+UVA, in one occasion under PAR+UVA+UVB, always absent from PAR. Crouania
was absent from the PAR+UVA treatment at all dates and depths.

Table 2: Filamentous macroalgal species

Rhodophyceae
Phaeophyceae
Chlorophyceae

Acrochaetium
daviesii
Dasya rigidula
Colpomenia
peregrina
Acetabularia
acetabulum

Alsidium
helmidochorton
Erythrotrichia
carnea
Dictyota
linearis
Bryopsis
pennata

Antithamnion
cruciatum
Falkenbergia
rufolanosa
Giffordia
mitchellae
Cladophora
coelothrix

Antithamnion
heterocladum
Fosliela
farinosa
Giffordia
granulosa
Cladophora
dalmatica

Aphanocladia
stichidiosa
Gelidiella
pannosa
Gigardua
sphacelarioides
Cladophora
pellucida

Antithamnion
tenuissimum
Gelidium
latifolium
Padina pavonica
Enteromorpha
ahleriana

Calithamnion
corymbosum
Goniotrichum
alsidii
Sphacelaria
plumula
Enteromorpha
clathrata

Centroceras
clavulatum
Goniotrichum
cornu-cervi
Sphacelaria
tribuloides
Enteromorpha
compressa

Ceramium
byssoideum
Griffithsia
tenuis
Stypocaulon
scoparium
Enteromorpha
multiramosa

Ceramium
cinabarium
Herposiphonia
tenella

Ulva curvata

Ceramium
cingulatum
Heterosiphonia
wurdemanni

Ceramium
circinatum
Jania rubens

Ceramium
diaphanum
Laurencia
papilosa

Ceramium
taylori
Lophosiphonia
cristata

Ceramium
tenuissimum
Lophosiphonia
scopulorum

Ceramium
tenerrimum
Plocamium
cartilagineum

Chondria
tenuissima
Polysiphonia
elongata

Chroodactylon
ornatum
Polyisiphonia
banyulensis

Compsothamnion
thuyoides
Pterosiphonia
parasitica

Coralina
granifera
Rhodophylis
divaricata

Crouania
atenuata

Specific remarks: In March (Table 3), five species (Gelidiella, Fosliella,
Polysiphonia, Cladophora, Giffordia) were present in most treatment combinations.
Giffordia was the most abundant. Lophosiphonia was randomly present at very low
numbers in all treatments. Heterosiphonia and Sphacelaria were present at
very low numbers only under PAR (Heterosiphonia at 0.5 and 1.0 m; Sphacelaria
at 1.0 and 1.5 m.) Crouania and Jania were abundant under PAR+UVA+UVB,
absent from PAR+UVA, and present at low numbers under PAR.

In April (Table 4), Heterosiphonia was again present only under PAR at 0.5 m. Crouania
and Acetabularia were present in low numbers under PAR+UVA+UVB and PAR and absent
from PAR+UVA. Lophosiphonia, Gelidiella, Jania and Fosliella
were present in most treatment combinations in relatively small numbers, while Giffordia,
Polysiphonia, Cladophora, Sphacelaria were more abundant.

Table 3: MARCH (9 months)

Species
PAR+UVA+UVB
PAR+UVA
PAR

depth (m)
0.5
1.0
1.5
0.5
1.0
1.5
0.5
1.0
1.5

Crouania
attenuata
+
++
++
-
-
-
-
+
+

Gelidiella
pannosa
+++
+
++
+
+
++
-
+
+

Jania rubens
++
+
+
-
-
-
+
-
-

Fosliella
farinosa
+
+
+
+
+
+
-
+
+

Polysiphonia elongata
+
+
+
++
++
+
+++
-
++

Heterosiphonia wurdemanni
-
-
-
-
-
-
+
+
-

Laurencia papilosa
++
-
-
+++
-
-
-
-
-

Cladophora pellucida
+
+
+
++
-
+
++
+++
++

Giffordia michellae
+++
+++
+++
+++
+++
+++
+++
+++
++

Lophosiphonia cristata
+
-
-
-
-
+
-
+
-

Acetabularia acetabulum
-
-
-
-
-
-
-
-
-

Sphacelaria tribuloides
-
-
-
-
-
-
-
+
+

Table 4: APRIL (10 months)

Species
PAR+UVA+UVB
PAR+UVA
PAR

depth (m)
0.5
1.0
1.5
0.5
1.0
1.5
0.5
1.0
1.5

Crouania attenuata
++
-
-
-
-
-
++
+
+

Gelidiella pannosa
+
+
-
+
+
-
+
++
++

Jania rubens
+
+
-
-
+
-
+
+
+

Fosliella farinosa
+
+
-
-
+
+
+
+
+

Polysiphonia elongata
+
++
++
+
++
++
-
+
-

Heterosiphonia wurdemanni
-
-
-
-
-
-
+
-
-

Laurencia papilosa
-
-
-
+++
-
-
-
-
-

Cladophora pellucida
++
+++
++
+
+
++
+
++
+++

Giffordia michellae
+++
++
+
++
+++
++
+++
+++
+

Lophosiphonia cristata
-
+++
++
-
+
-
+
++
++

Acetabularia acetabulum
-
+
-
-
-
-
+
-
++

Sphacelaria tribuloides
+
+
+
+
++
++
+
+
++

Table 5: JUNE (12 months)

Species
PAR+UVA+UVB
PAR+UVA
PAR

depth (m)
0.5
1.0
1.5
0.5
1.0
1.5
0.5
1.0
1.5

Crouania attenuata
-
-
-
-
-
-
-
+
+

Gelidiella pannosa
+++
++
+++
+++
+++
+++
+
+++
+++

Jania rubens
+
+
+
+
+
+
+
+
++

Fosliella farinosa
+
+
+
+
+
+
+
+
+

Polysiphonia elongata
+
++
+
++
+
+
+
+
+

Heterosiphonia wurdemanni
-
+
+
+
+
+
+
+
+

Laurencia papilosa
-
-
-
+
-
-
-
-
-

Cladophora pellucida
++
++
++
+
+
+
++
+
+

Giffordia michellae
+
+
-
+
+
+
++
+
++

Lophosiphonia cristata
+
++
+
++
+
+
+
+
+

Acetabularia acetabulum
+++
++
++
++
++
+
++
++
+

Sphacelaria tribuloides
++
+++
++
+
+
+
+++
+++
+++

(+): Relative abundance 0<5%; (++) >5-20%; (+++) >20%

In June (Table 5), Crouania was present only under PAR in low numbers. All other
species were present in most light and depth treatments at moderate-high numbers. The most
abundant algae were Gelidiella and Acetabularia.

Multivariate analyses indicated clear seasonal trend in community structure (figs.2,
3). June 1996 samples form a distinct group, while the separation between March and April
is less clear. Some clustering of light and/or depth treatments can be observed. However,
the effects of these factors on community composition are not consistent. For example, the
three PAR treatments group together, but a UVB treatment is also present (Fig 2: cluster
I); cluster II consists of five PAR treatments, one UV-A and one UV-B; cluster III
includes six UV-A and UV-B treatments, 1.0 and 1.5 meters, and one 'stranger' (PAR, 0.5
m).

Production of screening pigments

At the end of the growth period (12 months), samples were taken from each light regime
and pigments were extracted in methanol. The absorption spectra of the methanol extracts
were taken (Fig. 4) and the ratio between the chlorophyll peak at 666 nm and the
mycosporine peak at 336 nm was determined (Table 6). High ratios indicate increased
mycosporine content. Mycosporine content correlates both with spectral composition and
amount of UV radiation (Table 6). At 0.5 m, mycosporine content was highest under the
PAR+UV-A+UV-B treatment and lowest in the PAR treatment. In addition, in the PAR+UV-A+UV-B
treatment, mycosporine content decreased with depth, while in the PAR treatment it
remained rather constant. In the PAR+UVA treatment, mycosporine content decreased sharply
from 0.5 to 1.0 m.

Figure 4: Absorbance spectrum of methanol extracts from the macroalgal
assemblages (12 months, 0.5 m). The peaks at 336 and 666 nm correspond to mycosporine and
chlorophyll content. (Curves normalized over chlorophyll content.)

Table 6: Ratio of the absorption peaks at 336 nm and 666 nm in macroalgal
assemblages (mean values of four samples).

Depth
UVA + UVB + PAR
UVA + PAR
PAR

0.5m
3.21
3.17
2.68

1.0m
2.73
1.82
2.78

1.5m
2.06
2.11
2.64

Discussion

Naturally occurring UV radiation did not have any negative effects on standing crop. In
one case (April), the PAR treatment at 1.5 m had a lower standing crop than both the
PAR+UV-A+UV-B and the PAR+UV-A treatments at 0.5 (Fig. 2). This suggests that inhibition
due to light attenuation in the water column is more significant than inhibition due to
UVR.

Community analysis revealed seasonal patterns in the composition of the algal
assemblages. The distribution of certain species seems to be related to light treatment.
However, overall community structure did not correlate clearly with light treatment.
Previous studies have shown that although UV exposure affects the structure of diatom
assemblages during early primary succession, the differences disappear within 6 weeks^20,21,22.

The absence of UV effects can be explained by a) the wide seasonal fluctuations in
solar incidence, and b) the increased mycosporine production by the UV-exposed algae.

Solar incidence varied dramatically within the course of the year. Even during the four
month sampling period (March 96 – June 96) the total dose for the 3 bands of the
solar spectrum increased by a factor greater than 2 (Fig. 1). Spectral composition also
changes significantly with time of the year (see max/min ratios of the dose of three bands
under 'Results, Light doses'). Such complex patterns of exposure and spectral composition
challenge the predictive value of results obtained from constant, short-term exposure of
organisms in controlled laboratory experiments²³.

Screening pigment content correlated with light treatment. UV-A and UV-B radiation
induced mycosporine production, providing a protection and adaptation mechanism against
changes in light intensity and spectral composition.

In conclusion, the deleterious effects of UVR demonstrated in laboratory experiments
are often not supported by the findings of field studies. Although the UV ecology and
physiology of certain species of macroalgae deserves further investigation, adverse UV
effects, if they exist, can be masked by the overwhelming influence of other environmental
factors such as season and natural light fluctuations, as well as physiological adaptation
mechanisms of the organisms exposed.

Acknowledgments

This study has been funded by EC grants EV5V-CT94-0425 to R.S. and ENV4-CT96-0191 to
D.-P.H. (DG-XII, Environment Programme). The authors are grateful to Dr. I. Bittis for his
help on macroalgae identification.

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