Journal of Oceanography, Vol. 56, pp. 399 to 408, 2000
Variability in the Relative Penetration of Ultraviolet
Radiation to Photosynthetically Available Radiation
in Temperate Coastal Waters, Japan
VICTOR S. KUWAHARA1*, TATSUKI T ODA1, KOJI HAMASAKI 2, T OMOHIKO KIKUCHI 3
and SATORU TAGUCHI 1
1
Faculty of Engineering, Soka University, 1-236 Tangi-cho, Hachioji, Tokyo 192-8577, Japan
Faculty of Applied Biological Science, Hiroshima University,
1-4-1 Kagamiyama, Higashi-Hiroshima 739-8528, Japan
3
Faculty of Education and Human Sciences, Yokohama National University,
79-2 Tokiwadai, Hodogaya, Yokohama 240-0067, Japan
2
(Received 8 February 1999; in revised form 7 December 1999; accepted 11 December 1999)
UVR and PAR wavelengths are attenuated to different extents within the water column, causing variations in spectral composition with depth. The present investigation (a) describes the variability of UVR and PAR penetration at a station in the
temperate coastal waters of Sagami Bay and determines (b) the characteristics of
relative UVR penetration to the euphotic zone. Examination of the seasonal irradiance profile measurements indicated eight measurements displaying two distinct attenuation coefficients (Kd) for specific UVR wavelengths and PAR. The two attenuation coefficients observed from specific wavelengths in the water column may be caused
not only by chlorophyll pigments, but also by dissolved organic material in the upper
layer. The 1% depth of surface UVR at 305, 320, 340, and 380 nm averaged 10.8 ± 5.7,
14.9 ± 9.5, 19.8 ± 12.1, and 30.4 ± 17.6 m, respectively. The depth of euphotic layer
displayed less variability averaging 62 ± 15 m throughout the entire study. Relative
UVR penetration within the euphotic zone averaged 17.8 ± 8.1, 22.9 ± 10, 30.5 ± 13.8,
and 46 ± 46.9% for 305, 320, 340, and 380 nm, respectively. A large variation of the
relative transmission of UVR within the euphotic zone was found although the spectral composition was relatively stable in the air throughout the study.
1. Introduction
The rapid global depletion of the stratospheric ozone
layer has caused concern to the effects increased ultraviolet radiation (UVR) on the marine ecosystem (Prezelin
et al., 1994; Roy et al., 1994; Smith and Cullen, 1995).
Extensive studies demonstrated that ultraviolet radiationB (UVB; 280–320 nm) reaching the sea surface was hazardous to marine phytoplankton by damaging DNA, impairing photosynthesis and nutrient uptake, inhibiting
motility and orientation, and decreasing species diversity
(Cullen and Lesser, 1991; Behrenfeld et al., 1992, 1995;
Helbling et al., 1992, 1994; Bothwell et al., 1993; HolmHansen et al., 1993; Arrigo, 1994; Karentz, 1994; Prezelin
et al., 1994; Roy et al., 1994; Vernet et al., 1994). Ultraviolet radiation-A (UVA; 320–400 nm) and
Keywords:
⋅ Ultraviolet
radiation,
⋅ light penetration,
⋅ irradiance,
⋅ temperate coastal
water,
⋅ seasonal variation.
photosynthetically available radiation (PAR; 400–700 nm)
have been implicated in causing damage at intense levels
to phytoplankton communities but also in repair and adaptation processes (Karentz, 1994; Helbling et al., 1994;
Montecino and Pizarro, 1995; Peletier et al., 1996; Vernet
and Whitehead, 1996).
UVR is attenuated to different extents depending
upon wavelengths, causing change in UVR spectral distribution with depth in the water column. UVR penetration studies show that the 1% penetration of surface radiation in clear oceanic waters at 305 and 320 nm is close
to 35 and 50 m, respectively (Smith and Baker, 1981). In
Antarctica, the 1% depth for 308 and 320 nm reached
depths of 17.5 and 22 m, respectively (Helbling et al.,
1994) while in Hokkaido, Japan the 1% penetration of
surface UVB (320 nm) was shown to be from 1.3 to 16.0
m in coastal and oceanic waters, respectively (Taguchi et
al., 1993). In spite of these studies, the optical variability
of UVR penetration for various waters is not clear and
* Corresponding author. E-mail: [email protected]
Copyright © The Oceanographic Society of Japan.
399
further studies are necessary to understand the optical
properties within the water column that affect the penetration of UVR during the course of a year. In addition
to variability in penetration, the relative UVR penetration within the euphotic zone is poorly understood. The
1% penetration of surface PAR is often referred to as the
euphotic zone or compensation depth with regards to primary production. The depth to which surface UVR penetrates to 1% levels can be identified as the UVR effective layer (Morris et al., 1995; Williamson et al., 1996).
The variability of the spectral distribution of UVR within
the euphotic zone may determine whether phytoplankton
species will be damaged, capable of recovery, or capable
of adaptation from UVR exposure and this makes it specially important to study UVR penetration in marine ecosystems.
The objective of the present investigation is then
aimed to describe (a) the variability in UVR and PAR
penetration patterns in temperate coastal waters (Case II),
and to determine (b) the characteristics of relative UVR
penetration to the euphotic zone. We present the results
of time series observations of UVR and PAR from a representative Station M in the temperate coastal waters of
Sagami Bay, Japan.
2. Materials and Methods
2.1 Area investigated and time of sampling
Studies were conducted at Station M (35°09′ 49″ N,
139°10′ 33″ E, Depth of 120 m) off the Manazuru Peninsula in Sagami Bay (Fig. 1). Clear temporal fluctuations
due to influences from both sub-tropical and sub-polar
climates are found throughout the year, and monsoon
storm influences are known to occur due to mixture of
the two climate systems (Hogetsu and Taga, 1977). A total of 15 observations were conducted between July 1995
to December 1996 aboard the research vessel (R/V)
“Tachibana” of the Manazuru Marine Laboratory,
Yokohama National University. The survey on June 1996
was conducted aboard the R/V “Tansei-Maru”, Ocean
Research Institute, University of Tokyo (Table 1). All
surveys were conducted under visible clear-sky conditions
Table 1. Irradiance profiles which displayed a second attenuation coefficient. The number of data points (n, sample size) and
depth range used to derive each Kd are also shown. Numbers 1 and 2 at the shoulder of respective wavelengths represent clear
changes in the attenuation coefficient. na—indicates data not available.
400
V. S. Kuwahara et al.
while December 7, 1995 and August 12, 1996 were conducted during partly cloudy conditions.
2.2 Measurement of solar irradiation
Solar irradiation was measured using the PUV-500
submersible radiometer and the PUV-510 surface radiometer (Biospherical Instruments, Inc.) which provide
measurements of cosine-corrected downwelling irradiance. The instruments were designed to measure absolute UVR irradiance values with 10-nm bands centered
at 305, 320, 340, and 380 nm for UVR and 400–700 nm
for PAR. The mean surface irradiance was determined
from the data collected during the underwater profile
measurements. The submersible unit also measured depth
and temperature.
Irradiance profiles down to 80 m depth (at 0.5 m per
second) were conducted to determine the attenuation of
UVR and PAR. Data were collected at 1-second intervals
during the profiling. Measured irradiance profiles of
down-cast and up-cast were recorded. All surface and
profile casts were conducted within 3 hours of solar noon
during which special attention was paid to shadow from
the ship. Dark corrections, as described by Biospherical
Instruments, were conducted prior to every profile. The
sub-surface radiometer was always lowered into the water prior to measurements to minimize temperature ef-
fects. Current drag and tilt of the submersible sensor was
controlled to be minimal during the study. Special attention was also given to the rate at which the radiometer
was lowered and raised for each profile.
2.3 Diffuse attenuation coefficients
Data was analyzed in order to remove data points
which were either outside the detection limit of the radiometers sensors, or highly scattered which limited any
linear regression analysis. Diffuse attenuation coefficients
(Kd) for downwelling irradiance at each wavelength were
then determined from the slope of the linear regression
of natural logarithm of downwelling irradiance at each
respective wavelength against depth assuming that solar
irradiance reduces exponentially,
Ed ( z ) = Ed ( −0)e − K d z
(1)
where E d(z) is the downwelling irradiance at depth z, and
Ed (–0) is the downwelling irradiance just below the surface. The method described here provides mean estimates
of Kd across a wavelength specific path length that is the
distance from the surface to the depth at which the signal
falls below the detection level in the water column. On
some occasions the acquired irradiance displayed a second Kd for 320, 340, 380 nm, and PAR. In other words,
Fig. 1. Map of Sagami Bay and location of Station M.
Seasonal UVR Penetration
401
the exponential reduction of irradiance measurements
could be identified as two separate attenuation coefficients. Wavelengths which displayed the second Kd were
isolated as separate linear regression plots and identified
as numbers 1 and 2 at the shoulder of the respective wavelengths (Table 1). Irradiance sample size used to determine all Kd values was highly variable and dependent
upon wavelength but never less than 10 (n > 10). The
estimated Kd derived from the downcast and upcast used
as the final Kd value since the difference of the two casts
was less than 1%.
From the Kd values derived as above, 1% attenuation depth for each respective wavelength was then estimated using Eq. (1). Whenever the depth of the light
measurements did not extend to calculated 1% depths,
the same attenuation coefficient was applied to the layer
below detection limits. The calculated 1% depth for PAR
was defined as the “euphotic depth” while the relative
1% depth for specific UVR wavelengths was defined as
the effective depth of UVB and UVA penetration. In the
case of a second Kd value, both attenuation coefficients
were used to determine the 1% attenuation depth. The
percent depth of the effective UVR (EZ P) in the euphotic
depth was determined by,
EZ P = [UV1% (λ)]/[PAR1%]·100
2.4 Analysis of chlorophyll a pigments
Water samples were collected from depths of 0, 10,
20, 30, 50, and 75 m with 5L Niskin bottles for analysis
of chlorophyll a. Duplicate sub-samples of 200 ml from
each depth were filtered onto Whatman GF/F glass fiber
filters under subdued light. Filters were then stored in
opaque glass vials pre-filled with 10 ml N,Ndimethylformamide (DMF) for 24h to extract pigments
(Suzuki and Ishimaru, 1990). Concentrations of chloro-
(2)
where UV 1% is the 1% attenuation depth for UVR at a
given wavelength ( λ) and PAR1% is the 1% attenuation
depth for surface PAR.
Fig. 2. Seasonal fluctuation of temperature (°C) at Station M
from June 1995 to December 1996. Underline indicates
unavailable data.
Fig. 3. Seasonal fluctuation of chlorophyll a concentration (mgChla m–3) and sampling depths at Station M from June 1995 to
December 1996. Contour in May and June 1996 in the upper 10 m layer was not made due to higher concentrations of
chlorophyll a at 15 mgChla m–3. Dashed line indicates the 1% penetration depth of surface PAR. Underline indicates unavailable data.
402
V. S. Kuwahara et al.
phyll a were determined fluorometrically using a Turner
Design, Model 10-AU according to Holm-Hansen et al.
(1965).
3. Results
3.1 Water column conditions
The water column was thermally stratified from June
to September 1995 with the warmest surface temperature
at 25.9°C on August 18, 1995 (Fig. 2). The water column
was thermally well mixed to 16°C during winter from
December 1995 to January 1996. Stratification began to
develop again in April 1996 and was observed to a maximum depth of 60 m in October 1996.
Seasonal surface chlorophyll a concentrations averaged 1.45 mgChla m–3 between July to August 1995 but
decreased to as low as 0.284 mgChla m–3 between September 1995 and January 1996 (Fig. 3). Chlorophyll a
Fig. 4. Seasonal variation of surface UVR and PAR (䊐 305, 䉫 320, 䉭 340, 䊊 380 nm, and * PAR) obtained during the vertical
profiling (20 minutes) of underwater UVR and PAR at Station M from June 1995 to December 1996. Underline indicates
unavailable data.
Fig. 5. Seasonal variation of average surface UVR/PAR ratio (䊐 305, 䉫 320, 䉭 340, and 䊊 380 nm) obtained during the vertical
profiling of underwater UVR and PAR at Station M from June 1995 to December 1996. Underline indicates unavailable data.
Seasonal UVR Penetration
403
concentrations decreased gradually and reached 15
mgChla m–3 on June 18, 1996. After this maximum, concentrations decreased once again and during the winter
of 1996 low concentrations of 0.60 mgChla m –3 were
measured from the surface layer to 30 m.
3.2 Downwelling UVR at the ocean surface
The highest UVR values for 380, 340, 320, and 305
nm were 0.77, 0.58, 0.30, and 0.05 µWm–2nm–1, respectively on June 17, 1995 (Fig. 4). Lowest UVR values were
recorded on December 22, 1995 and were 0.18, 0.13, 0.05,
Fig. 6. Vertical profiles of the percent penetration of PAR and UVR (—), temperature (- - -), and chlorophyll a concentration (䊊)
on December 7, 1995 (A), July 18, 1995 (B), August 18, 1995 (C), and July 13, 1996 (D). The percent penetration of UVR and
PAR during December (A) showed one attenuation coefficient while July (B) displayed a second attenuation coefficient for
PAR. 305 nm in December (A) was unavailable due to low irradiance and noise. August (C) showed a second attenuation
coefficient below 32 m depth in PAR (not shown in figure) and UVR displayed a second slope at 380 nm and 340 nm. July (D)
also displayed a second attenuation coefficient in PAR and UVR with the exception of 305 nm and 320 nm.
404
V. S. Kuwahara et al.
and 0.001 µWm–2nm–1 for 380, 340, 320, and 305, respectively. Surface PAR irradiance showed similar temporal fluctuations (Fig. 4). UVR/PAR irradiance ratios
were calculated to determine their seasonal variability.
The mean for each ratio at 305, 320, 340, and 380 nm to
PAR was 19 ± 10, 136 ± 18, 275 ± 18, and 364 ± 15
µW/µE, respectively (Fig. 5). The coefficient of variation (%) for those ratios was 50, 13, 6, and 4, respectively.
3.3 Attenuation coefficients
Detailed analysis of the 15 profiles collected exhibited the following three vertical patterns of Kd. The first
pattern, represented by December 7, 1995, displayed one
clear Kd for each respective UVR wavelength and PAR
(Fig. 6A). The water column during this month was well
mixed with average chlorophyll a concentrations of 0.356
mgChla m –3. The second pattern, as illustrated by July
18, 1995, displayed UVR wavelengths having one Kd and
UVR wavelengths were quickly attenuated near the surface. In contrast, PAR displayed two Kd (Fig. 6B). The
water column during this month was thermally stratified
and surface chlorophyll a concentrations reached 3.65
mgChla m –3. The third pattern, depicted by August 18,
1995 and July 13, 1996, showed both UVA and PAR wavelengths having two Kd values (Figs. 6C and D). In addition to the first Kd observed within 5 m for UVR and
within 30 m for PAR, UVR wavelengths displayed a second Kd within 10 m of the surface while a second Kd for
PAR was found below the thermocline at 32 m (Table 1).
The water column on August 18, 1995 was thermally
stratified to 20 m and average chlorophyll a concentrations of 0.309 mgChla m–3 were observed. On July 13,
1996 a temperature decrease from 22.8 to 20.8°C was seen
within the first 5 m and chlorophyll a concentrations
reached 3.02 mgChla m–3 at the 10 m depth. UVA wavelengths and PAR showed a second Kd at 5.5 m and 8 m,
respectively. Examination of the 15 profile measurements
showed that 5 winter and 2 spring measurements displayed
a single Kd while the 6 summer and 2 autumn measurements displayed two Kd (Table 2).
Using Kd from Eq. (1), the relative 1% depth was
calculated for all UVR wavelengths and PAR. The 1%
depth was calculated from the surface irradiance for wavelengths which showed a second Kd. The 1% depth of UVR
was highly variable at all wavelengths (C.V. > 53%) (Ta-
Table 2. Attenuation coefficients (Kd) and the 1% penetration depth of UVR wavelengths (305, 320, 340, and 380 nm) and PAR.
The first attenuation coefficient is shown for month with two Kd and the 1% depths were calculated from the surface irradiance. na—indicates data not available.
(a)
Months with second Kd in PAR.
Months with second Kd in UVA.
(c)
1% depths calculated from surface irradiance.
(b)
Seasonal UVR Penetration
405
Fig. 7. Seasonal fluctuation of the percent penetration of UVR
(䊐 305, 䉫 320, 䉭 340, and 䊊 380 nm) (EZ P) within the
euphotic zone (1% penetration of PAR) at Station M from
June 1995 to December 1996. Underline indicates unavailable data.
ble 2). PAR showed the least variability averaging 60.3 ±
14.9 m (C.V. = 25%) throughout the entire study. The
shallowest and deepest 1% penetration of UVB (320 nm)
and UVA (380 nm) was found on August 12, 1996 (4.6
and 7.6 m) and December 7, 1995 (38.4 and 74.4m), respectively.
3.4 Relative UVR penetration within the euphotic zone
The lowest relative penetration of UVR against the
1% depth of PAR (EZ P) was 6, 7, 9, and 14% for 305,
320, 340, and 380 nm, respectively in July 1995 (Fig. 7).
The highest values of EZ P were 41, 54, and 80% for 320,
340, and 380 nm, respectively on December 7, 1995.
During the summer of 1995, UVR increased from 6–16%
for UVB wavelengths and 9–46% for UVA wavelengths.
EZ P varied little from September 1995 to May 1996 and
averaged 32 ± 5% and 64 ± 6% for UVB and UVA, respectively. From May to July 1996 it showed a gradual
decrease from 27–10% and from 56–26% in the UVB and
UVA range, respectively. EZ P gradually increased again
in September 1996 and reached a maximum of 24% at
305 nm, 32% at 320 nm, 43% at 340 nm, and 64% at 380
nm in December 1996. Relative UVR penetration displayed an average of 17.9 ± 7.8 (C.V. = 44%), 23.3 ±
10.7 (C.V. = 46%), 31.5 ± 13.6 (C.V. = 43%), and 49.2 ±
19.8% (C.V. = 40%) for 305, 320, 340, and 380 nm, respectively.
4. Discussion
UVR and PAR irradiance at the ocean surface displayed temporal variations that were dependent upon the
406
V. S. Kuwahara et al.
season, i.e. elevation of the sun (Fig. 4). The ratio of UVR
to PAR reaching the surface is known to change due to
distinct absorption of ultraviolet radiation by ozone (Kerr
and McElroy, 1993). The present study showed that the
surface UVR/PAR ratio at Station M was relatively constant with time (Fig. 5). This suggests that this region
was less effected by ozone and atmospheric conditions
(i.e. aerosol, cloud coverage, and water vapor) which are
known to change surface UVR/PAR ratios.
In the present study the relative 1% depth of surface
UVR during the winter was comparable to those observed
for clear waters by Smith and Baker (1979) and Kirk
(1994a), while during the summer the 1% depth of surface UVR was comparable to waters of high chlorophyll
concentrations (Kirk, 1994a; Dunne and Brown, 1996)
(Table 2). The variability of the 1% surface UVR penetration (C.V. > 53%) was much larger than that of PAR
(C.V. = 23%) (Table 2). This suggests that UVR penetration was more influenced by changing water column conditions than PAR.
The most striking result of the present study was the
high variability but regularity of relative UVR penetration within the euphotic zone (1% depth of PAR) (Fig.
7). Relative UVB and UVA penetration fluctuated during
the present study from 6 to 41% and from 9 to 80%, respectively. These temporal variations further support the
notion that UVR penetration may not be clearly determined from PAR penetration alone (Dunne and Brown,
1996). Laurion et al. (1997) have suggested that in freshwater ecosystems, changes in the UVR/PAR ratio may be
due to variations in dissolved organic material (DOM).
Our results show that the distribution of light within the
water column was wavelength dependent and highly sensitive to the vertical distribution of attenuating materials,
which in turn varied seasonally.
Although the optical condition of the water is traditionally considered homogeneous, our region of study
revealed abrupt changes in Kd in a water column (a second attenuation coefficient) (Table 1). A second Kd for
PAR was often observed near the thermocline and UVR
also displayed a second Kd on two occasions (Figs. 6C
and D). Although chlorophyll a concentrations lower than
0.4 mgChla m–3 were observed throughout the water column, a second Kd at 340 and 380 nm were detected in the
water column on August 18, 1995 within the thermocline.
However, due to detection limitations of the present instrument, we were not able to observe a second attenuation coefficient at 305 and 320 nm, as penetration deeper
than 5 m were not detected. This suggested that specific
UVR absorbing materials other than phytoplankton might
have contributed to sub-surface attenuation of light. Redtide and diatom blooms are known to be significant in
the surface layers above the thermocline (Hogetsu and
Taga, 1977) from the spring to summer, a period in our
Fig. 8. Relationship between the months with a single attenuation coefficient (Kd) of irradiance and the surface chlorophyll a
concentration at Station M from June 1995 to December 1996. Liner regression fit were significant (P < 0.05) for all wavelengths. Months that showed a second attenuation coefficient were not included in analysis.
study when a second attenuation coefficient was seen.
These species are particularly effective in absorbing UVR
wavelengths due to the presence of mycosporine-like
amino acid compounds (Karentz, 1994; Vernet and Whitehead, 1996). These blooms and their extracellular products released and degraded following the summer, may
have contributed to the attenuation of UVR (Antia et al.,
1991).
The focus of the present study was also to identify
the variability in UVR penetration with respect to PAR.
Surface chlorophyll a concentrations were compared with
Kd values of UVR and PAR to determine their relationship (Fig. 8). The results showed a significant relationship between all UVR wavelengths having a single attenuation coefficient only (305 nm, r = 0.79, P < 0.05;
320 nm, r = 0.85, P < 0.01; 340 nm, r = 0.82, P < 0.01;
380 nm, r = 0.81, P < 0.01; PAR, r = 0.85, P < 0.01).
However, no significant relationship was observed during the months that displayed a second attenuation coefficient. This may suggest that whenever a second attenuation coefficient was observed non-chlorophyll-like material was more dominant than chlorophyll a in the surface layer. In addition to the release and degradation of
extracellular products mentioned above, terrestrial derived
DOM contribution from rainfall (Hogetsu and Taga, 1977;
Kirk, 1994b; Zweifel et al., 1995) may have also contributed since the rainy season usually occurs during the summer in the area of study. Our results show that UVR penetration within the euphotic zone is dependent upon season and highly variable although further studies are
needed to elucidate the factors that contribute to this variability.
Acknowledgements
We thank our colleagues from the Soka University,
Japan laboratory for their assistance at the field and laboratory. We also thank the captain and crew of the R/V
Tansei-Maru of the Ocean Research Institute, University
of Tokyo for their excellent assistance. We are particularly grateful to Y. Asakura of the National University of
Yokohama for the facility of the Manazuru Marine Laboratory. We also thank M. Kishino and H. Gomes for comments on the earlier version of this manuscript. This study
was partially supported by a grant from the Environmental Agency of Japan.
References
Antia, N. J., P. J. Harrison and L. Oliveira (1991): The role of
dissolved organic nitrogen in phytoplankton nutrition, cell
biology and ecology. Phycologia., 30, 1–89.
Arrigo, K. R. (1994): Impact of ozone depletion on
phytoplankton growth in the southern ocean: Large-scale
spatial and temporal variability. Mar. Ecol. Prog. Ser., 114,
1–12.
Behrenfeld, M. J., J. T. Hardy and H. Lee, II (1992): Chronic
effects of ultraviolet-B radiation on growth and cell volume of Phaeodactylum tricornutum (Bacillariophyceae). J.
Phycol., 28, 757–760.
Behrenfeld, M. J., D. R. S. Lean and H. Lee, II (1995): Ultraviolet-B radiation effects on inorganic nitrogen uptake by
natural assemblages of oceanic plankton. J. Phycol., 31, 25–
36.
Seasonal UVR Penetration
407
Bothwell, M. L., D. Sherbot, A. C. Roberge and R. J. Daley
(1993): Influence of natural ultraviolet radiation on lotic
periphytic diatom community growth biomass accrual, and
species composition: Short term versus long-term effects.
J. Phycol., 29, 24–35.
Cullen, J. J. and M. P. Lesser (1991): Inhibition of photosynthesis by ultraviolet radiation as a function of dose and dosage rate: Results for a marine diatom. Mar. Biol., 111, 183–
190.
Dunne, R. P. and B. E. Brown (1996): Penetration of solar UVB
radiation in shallow tropical waters and its potential biological effects on coral reefs; results from the central Indian Ocean and Andaman Sea. Mar. Ecol. Prog. Ser., 144,
109–118.
Helbling, E. W., V. Villafane, M. Ferrario and O. Holm-Hansen
(1992): Impact of natural ultraviolet radiation on rates of
photosynthesis and on specific marine phytoplankton species. Mar. Ecol. Prog. Ser., 80, 89–100.
Helbling, E. W., V. Villafane and O. Holm-Hansen (1994): Effects of ultraviolet radiation on Antarctic marine
phytoplankton photosynthesis with particular attention to
the influence of mixing. Antarc. Res. Ser., 62, 207–227.
Hogetsu, K. and N. Taga (1977): Suruga Bay and Sagami Bay.
p. 31–172. In JIBP Synthesis, Productivity of Biocenoses in
Coastal Regions of Japan, Vol. 14, ed. by K. Hogetsu, M.
Hatanaka, T. Hanaoka and T. Kawamura, University of Tokyo Press, Tokyo.
Holm-Hansen, O., C. J. Lorenzen, R. N. Holmes and J. D. H.
Strickland (1965): Flurometric determination of chlorophyll.
J. Cons. Perm. Int. Expl. Mer., 30, 3–15.
Holm-Hansen, O., E. W. Helbling and D. Lubin (1993): Ultraviolet radiation in Antarctica: Inhibition of primary production. Photochem. Photobiol, 58, 567–570.
Karentz, D. (1994): Ultraviolet tolerance mechanisms in Antarctic marine organisms. Antarc. Res. Ser., 62, 93–110.
Kerr, J. B. and C. T. McElroy (1993): Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion. Science, 262, 1032–1034.
Kirk, J. T. O. (1994a): Optics of UV-B radiation in natural waters. Ergeb. Limnol. Oceanogr., 43, 1–16.
Kirk, J. T. O. (1994b): Light and Photosynthesis in Aquatic
Ecosystems. 2nd ed., Cambridge Univ. Press, Cambridge,
509 pp.
Laurion, I., W. F. Vincent and D. R. S. Lean (1997): Underwater ultraviolet radiation: Development of spectral models
for northern high latitude lakes. Photochem. Photobiol., 65,
107–114.
Montecino, V. and G. Pizarro (1995): Phytoplankton acclimation
and spectral penetration of UV irradiance off the central
Chilean coast. Mar. Ecol. Prog. Ser., 121, 261–269.
Morris, D. P., H. Zagarese, C. E. Williamson, E. G. Balseiro,
408
V. S. Kuwahara et al.
B. R. Hargreaves, B. Modenutti, R. Moeller and C.
Queimalinos (1995): The attenuation of solar UV radiation
in lakes and the role of dissolved organic carbon. Limnol.
Oceanogr., 40, 1381–1391.
Peletier, H., W. W. C. Gieskes and A. G. J. Buma (1996): Ultraviolet-B radiation resistance of benthic diatoms isolated
from tidal flats in the Dutch Wadden Sea. Mar. Ecol. Prog.
Ser., 135, 163–168.
Prezelin, B. B., N. P. Boucher and R. C. Smith (1994): Marine
primary production under the influence of the Antarctic
ozone hole: Icecolors ’90. Antarc. Res. Ser., 62, 159–186.
Roy, C. R., H. P. Gies, D. W. Tomlinson and D. L. Lugg (1994):
Effects of ozone depletion on the ultraviolet radiation environment at the Australian stations in Antarctica, ultraviolet
radiation in Antarctica: Measurements and biological effects. Antarc. Res. Ser., 62, 1–15.
Smith, R. C. and K. S. Baker (1979): Biologically effective dose
transmitted by culture bottles in 14C productivity experiments. Limnol. Oceanogr., 25, 364–366.
Smith, R. C. and K. S. Baker (1981): Optical properties of the
clearest natural waters (200–800 nm). Appl. Opt., 20, 177–
184.
Smith, R. C. and J. J. Cullen (1995): Effects of UV radiation on
phytoplankton. p. 1211–1223. In U.S. National Report to
International Union of Geodesy and Geophysics 1991–1994.
Reviews of geophysics, supplement.
Suzuki, R. and T. Ishimaru (1990): An improved method for
determination of phytoplankton chlorophyll using N,NDimethylformamide. J. Oceanogr. Soc. Japan, 46, 190–194.
Taguchi, S., H. Saito and H. Kasai (1993): Characteristics of
ultraviolet radiation penetration in the sea and its effects
on marine phytoplankton community in the Western
Subarctic Pacific. p. 251–264. In The 13th UOEH International Symposium and 2nd Pan Pacific Cooperative Symposium on Impact of Increased UV-B Exposure on Human
Health and Ecosystem, ed. by Y. Kodama and S. D. Lee.
Vernet, M. and K. Whitehead (1996): Release of ultravioletabsorbing compounds by the red-tide dinoflagellate
Lingulodinium polyedra. Mar. Biol., 127, 35–44.
Vernet, M., E. A. Brody, O. Holm-Hansen and B. G. Mitchell
(1994): The response of Antarctic phytoplankton to ultraviolet radiation: Absorption, photosynthesis, and taxonomic
composition. Antarc. Res. Ser., 62, 143–158.
Williamson, C. E., R. S. Stemberger, D. P. Morris, T. M. Frost
and S. G. Paulsen (1996): Ultraviolet radiation in North
America lakes: Attenuation estimates from DOC measurements and implications for plankton communities. Limnol.
Oceanogr., 41, 1024–1034.
Zweifel, U. L., J. Wikner, A. Hagstrom, E. Lundberg and B.
Norrman (1995): Dynamics of dissolved organic carbon in
a coastal ecosystem. Limnol. Oceanogr., 40, 299–305.