Hydrobiologia 385: 2332, 1998.

1998 Kluwer Academic Publishers. Printed in the Netherlands.

23

Effects of ultraviolet radiation on primary productivity

in a high altitude tropical lake

Robert A. Kinzie III1 , Anastazia T. Banaszak2 & Michael P. Lesser3

1 HawaiiInstitute of Marine Biology, P.O. Box. 1346, Kaneohe, HI 96744, U.S.A.
2 Smithsonian Environmental Research Center, P.O. Box 28, Edgewater, MD 21037-0028, U.S.A.
3 Department of Zoology and Center for Marine Biology, University of New Hampshire, Durham, NH 03824, U.S.A.

Received 16 January 1997; in revised form 9 May 1998; accepted 29 July 1998

Key words: Ultraviolet radiation, primary productivity, tropical lakes

Abstract
The aquatic photosynthetic community in Lake Waiau (elev. 3980 m, lat. 19 480 N) is exposed to intense solar
ultraviolet radiation (UVR) due to the high altitude and low latitude. There is a strong negative effect of UVR on
photosynthesis both in the planktonic and benthic mat communities in the lake. The mats apparently receive some
protection from UVR-absorbing mycosporine-like amino acids (MAAs), while the planktonic primary producers
do not appear to have such protection and exhibit no net photosynthesis at levels of UVR characteristic of the lake
surface at midday. These forms may be meroplanktonic or rely on vertical mixing for protection from extended
periods of exposure to UVR.

Introduction There exists an extensive literature on the cellu-

General concern about the broad biological effects
of increasing UV-B (290320 nm) irradiances reach-
ing the Earths surface has increased following the
detection of biologically significant UVR effects in
the Antarctic where severe reductions in stratospheric
ozone have occurred (Dahlback et al., 1989, Smith et
al., 1992). This heightened concern is largely due to
some projections that an increase in UV-B radiation
(290320 nm) could become a significant factor in the
northern hemisphere at mid-latitudes (Madronich et
al., 1991; Mahlman, 1992) but especially at high alti-
tudes (Blumthaler & Ambach, 1990). Impacts ranging
from increases in human skin cancers and cataracts
(Setlow, 1974; Taylor, 1989) to a reduction in primary
production in marine (Buma et al., 1996; Caldwell,
1979; Helbling et al., 1992; Larkum & Wood, 1990;
Tevini & Teramure, 1989) and freshwater (Bothwell
et al., 1993, 1994; Gala & Giesy, 1991) systems
have been observed (see references in recent reviews:
Franklin & Forster, 1997; Hder, 1993; Hder &
Worrest, 1991).
lar and subcellular sites of UVR damage, but there
is much less known about responses at the organis-
mal level and even less at the level of the community
(Bothwell et al., 1993, 1994; Kelly, 1986; Lee &
Lowry, 1980; Worrest et al., 1981), What informa-
tion does exist about community level effects of UVR,
suggests that the impacts are complex and may be non-
intuitive (Bothwell et al., 1993, 1994; Newsham et
al., 1997; Williamson, 1995) with the possibility of
UV-A (320400 nm) conferring some protection from
the harmful effects of UV-B via photo-reactivation-
mediated repair processes (Quesada et al., 1995).
Tropical ecosystems have, even before any reduction
in stratospheric ozone, been exposed to greater UVR
fluxes than higher latitudes. This is due to a naturally
thinner ozone layer over low latitudes and the more
direct path of solar radiation through the atmosphere
near the equator (Frederick et al., 1989; Gleason et al.,
1993). Tropical aquatic organisms have been shown to
be sensitive to natural levels of UVR (Jokiel, 1980)
and to have protective mechanisms such as the pres-
ence of UVR-absorbing compounds which can be
24
produced in response to exposure to UVR (Banaszak
& Trench, 1995; Helbling et al., 1996; Kinzie, 1993).
A protective role for these compounds has been in-
ferred from their UVR-absorbing properties and their
logarithmic decrease in concentration with increasing
depth in corals (Dunlap et al., 1986; Kuffner et al.,
1995; Scelfo, 1984). The concentrations of these com-
pounds may also change after shielding from exposure
to UVR, or transplantation of organisms to shallower
habitats (Jokiel & York, 1982; Scelfo, 1984; Shick
et al., 1991). These UVR-absorbing compounds have
been identified as mycosporine-like amino acids (Dun-
lap & Chalker, 1986) and have been found in a wide
range of aquatic organisms including cyanobacteria,
phytoplankton, algae, invertebrates and vertebrates
from tropical to polar waters (Garcia-Pichel & Cas-
tenholz, 1993; Helbling et al., 1996; Karentz et al.,
1991).
The level of UVR actually reaching living organ-
isms depends on many factors. Even though all of the
Earths surface is below the stratosphere, the region
of maximum ozone concentrations, the troposphere
contains significant levels of UVR-absorbing materi-
als (Penkett, 1988). Work in high-altitude lakes has
demonstrated important UVR impacts even at tem-
perate latitudes (Caldwell, 1968; Rodhe et al., 1966).
Photoinhibition has been demonstrated in phytoplank-
ton communities in a high-altitude tropical lake (Neale
& Richerson, 1987). Diel studies of phytoplankton
photosynthesis in the high altitude (3803 m), tropical
Lake Titicaca show that the phytoplankton population
dominated by centric diatoms and filamentous chloro-
phytes is sensitive to photoinhibition. The onset of
photoinhibition occurs at around midday and extends
into the afternoon as determined by fluorescence mea-
surements (Neale & Richerson, 1987). The highest
levels of UVR currently reaching the Earths surface
would be expected at high elevations in the tropics
where the thin ozone layer, the direct solar path and
the reduction of overlying atmosphere would combine
to allow maximum exposure to UVR.
Lake Waiau, near the summit of Mauna Kea,
Hawaii, at 3980 m (Woodcock et al., 1966) is re-
ported as the highest lake in the US (Maciolek 1969).
Earlier studies described the geology and limnology
of this lake (Fan, 1978; Maciolek, 1969; Wentworth
& Powers, 1943; Woodcock, 1980). Massey (1978a,
b, 1981) reported on the diatom flora of Lake Waiau
and gave data on productivity that showed that while
there was a high standing crop, productivity was low.
She suggested that the low productivity could be due
to high light levels or to low nutrient concentrations
(Massey, 1978a,b 1981). Laws & Woodcock (1981)
noted a short-lived, but intense bloom of a chlorophyte
that temporarily replaced the numerically dominant
diatom flora during a drought.
During the summer of 1994, an opportunity to sur-
vey some photobiological aspects of Lake Waiau was
undertaken in conjunction with a course and workshop
on the effects of UVR in tropical ecosystems held at
the University of Hawaii at Manoa and the Hawaii
Institute of Marine Biology. The goals of the study
were to characterize the lake environment with respect
to solar radiation and to determine the impacts on the
primary producers in the lake.
Materials and methods
Site
Lake Waiau is located near the summit of Mauna Kea
(19 480 N, 155 290 W) the highest of the five vol-
canic peaks that make up the island of Hawaii. The
altitude is variously given as 3969, 3970 and 3980 m
(Maciolek, 1969; Woodcock, 1980; Fan, 1978; re-
spectively). The approximately 0.73-ha lake lies in
a shallow crater and has a rocky margin. Lake size
varies greatly with precipitation but its maximum di-
ameter is near 90 m and the maximum depth is about
3 m. Maciolek (1969, 1982) gives the most complete
description of the site and the lake characteristics.
This cold mono- or polymictic lake is ice covered
in winter, but no long-term record giving times of
freezing and thawing exists. The small drainage area
consists of barren alpine tundra (Neal 1939). Weather
is extreme with winds (recorded at the astronomical
observatories approximately 2.5 km from the lake
from January 1993 to December 1994) of 6480 kph
occurring 3.1% of the time and winds greater than
80 kph over 3.8% of the time. Mean wind velocity
during this 2-year period was 30 kph. Mean annual
air temperature was 22.6 C during the same period.
Lake water is typically isothermal with temperature
ranging from 0 to 13 C (Woodcock 1980). Maciolek
(1969) reported a pH of 7.27.3 and conductivity of
54121 S cm2 . In her extensive study of Lake Wai-
au, Massey (1978a,b, 1981) also reported on physical
conditions and presented data on dissolved inorganics.

Measurement of solar irradiance
Field work at the lake took place on July 1617
1994. July 16 was clear while on July 17 there were
afternoon clouds and rain. No photosynthesis mea-
surements were taken on the latter date. Spectral data
(300700 nm) were recorded at a depth of 5 cm us-
ing a LiCor LI-1800UW scanning spectroradiometer
(LiCor, Lincoln, NE) from noon, July 16 to noon,
July 17, 1994. The cosine-corrected collector and sen-
sors were programmed to scan from 300700 nm in
2-nm intervals hourly. For each measurement, three
scans were taken and the mean reported in units of
W m2 nm1 . Temperature was recorded during the
same period at 5 min. intervals using a submerged
HoboTemp (5 C to +37 C) recorder (Onset Com- method (Strickland & Parsons, 1972). Samples for
puter Corp.).
Solar radiation was also measured at Kaneohe
Bay on July 26, 1994 and represents the maximum
downwelling irradiances reaching sea level at 12:00
noon. Integrated values of biologically weighted UVR
(300400 nm) were calculated for Lake Waiau in
air and in water for noon time measurements and
Kaneohe Bay air measurements at noon for com-
parison. Biologically effective irradiances were deter-
mined using the DNA weighting function of Setlow
(1974), the chloroplast photoinhibition function of
Jones & Kok (1966), and the diatom photoinhibition
weighting function of Cullen et al. (1992).
Primary producers
Primary producers previously reported from the lake
were from several different phytoplanktonic taxa
(Massey, 1978b). We also noted dense cyanobacte-
rial/algal mats that completely covered the shallow
substratum on the upwind side of the lake. The mats
were more broken and less dense on the downwind
littoral benthos where water movement is greater. We
sampled phytoplankton by horizontally hand-towing a
15-cm diameter phytoplankton net (mesh size 45 m)
at the lake surface and at approximately 0.5 m depth.
Mats were sampled by hand. Samples were fixed in
10% formalin and flora were subsequently identified
to the lowest possible taxon.
Photosynthesis measurements
Primary production of the phytoplankton community
was measured using light/dark bottle methodology
employing BOD bottles made of UV-transmitting
25
quartz. The two dark bottles were wrapped in sev-
eral layers of black plastic tape. Three quartz bottles
with phytoplankton were placed under UV-opaque
polycarbonate, and three were placed under the
UVR-transparent chlorolfuorocarbon Aclar (Jokiel
& York, 1984). Mat photosynthesis was measured by
collecting pieces of mat and enclosing them in tightly
sealed plastic containers. Two of the containers had
tops fitted with plastic windows, one of polycarbon-
ate and one of Aclar. The third box was wrapped in
several layers of black plastic to serve as the dark
container. Both bottles and plastic containers were
held submerged under 5 cm of lake water during
the incubations to maintain ambient temperature. Oxy-
gen concentration was determined using the Winkler
oxygen determinations were taken at the beginning
of the incubations and after the approximately 2-h
incubations. Lake water samples were filtered onto
GF/F glass fiber filters and kept frozen for subsequent
analysis. Water column chlorophyll a (Chl a) was de-
termined fluorometrically after extraction in acetone.
At the end of the mat incubation, mats were frozen.
Subsequently mat area was determined gravimetri-
cally using tracings of the mats on heavy cardboard
which were then cut out and massed to the nearest 0.1
g. Chlorophyll a from the mats was extracted repeat-
edly in 90% acetone until no Chl a was detected in the
solvent. All extractions from a mat were pooled for de-
termination of total Chl a using the equation of Jeffrey
& Humphrey (1975). Mats plus all solvent were dried
first at room temperature to evaporate the solvent, then
at 60 C for 24 h and massed to obtain dry mass (DM).
Mats were then ashed at 500 C for 6 h and re-massed
to obtain ash free dry mass (AFDM). Nutrients in
the lake water were analyzed using methods modified
from Smith et al., (1981).
UVR-absorbing compounds
Algal samples were collected for determination of
concentrations of UVR-absorbing compounds. Ex-
traction and analysis of mycosporine-like amino acids
(MAAs) was performed according to the procedures
in Dunlap & Chalker (1986) as modified by Shick et
al. (1992) and Stochaj et al. (1994). MAAs were ex-
tracted in 100% high performance liquid chromatog-
raphy (HPLC)-grade methanol for 12 h at 20 C
and quantified using reverse-phase, isocratic HPLC.
MAAs were separated using a Brownlee RP-8 column
(spheri-5 4.6 mm ID 25 cm) protected with an RP-
26

Figure 1. Solar spectral irradiance (W m2 nm1 ) at Lake Waiau, Hawaii and at Kaneohe Bay. Each line represents the mean of three scans
from 300 to 700 nm at 2 nm intervals taken at the time noted. The scan at Kaneohe Bay was taken at noon. The scan labeled air was taken at
Lake Waiau in air.

Table 1. (A) Noon solar radiation in air (W m2 ) at Lake Waiau and Kaneohe Bay, (B) Ratios
of UVR to PAR and (C) Weighted integrals of UVR dose (W m2 )
(A) 300320 nm 300400 nm 400700 nm
Lake Waiau 4.668 69.97 475
July 16 11994
Kaneohe Bay 3.761 63.77 481
July 26 1994
(B) 300320 nm:PAR 300400 nm:PAR
Lake Waiau 9.93 103 0.147
Kaneohe Bay 7.82 103 0.133

(C) Setlow Cullen & Lesser Jones & Kok

DNA damage marine diatom photoinhibition
(1974) (1991) (1966)

Kaneohe Bay Air 0.0150 0.0032 16.774

Lake Waiau Air 0.0191 0.0035 17.779
Lake Waiau under 5 cm water 0.0051 0.0020 12.107

8 guard column (spheri-5 4.6 mm ID 3 cm) and an
aqueous mobile phase with 40% methanol and 0.1%
acetic acid (v:v) run at a flow rate of 0.6 ml min1 .
Peak detection was by UVR absorption at 313 and
340 nm using a Waters 440 absorbance detector and
confirmed on a Waters 990 Photodiode array detec-
tor. Peaks were calibrated against known standards
using co-chromatography, the ratio of absorbance at
313 and 340 nm, and by the maximal wavelength
of absorbance. Quantification was determined using
peak area integrations and calibration factors deter-
mined by analysis of the standards and in-line diode
array spectroscopy. MAA concentrations were nor-
malized to soluble protein (determined from an aliquot
of the methanol-extracted sample) and concentrations
expressed as nmol mg1 protein. Protein concentra-
tions were determined using the Lowry technique with
the Hartree modification (Hartree, 1972).
Results
Spectral irradiances reaching the lake surface recorded
hourly and at Kaneohe Bay at noon are shown in Fig-
ure 1. Table 1A lists the integrated values of visible
and UV clear sky solar radiation at Lake Waiau and
Kaneohe Bay. On the dates the measurements were
made, Lake Waiau received about 24% more UVR in
the 300320 nm range, and 10% more over the total
300400-nm range than Kaneohe Bay. Perhaps more
important are the differences in the relative contribu-
tion of UVR to the total solar radiance (Table 1B).
The ratio of UVR to PAR is 1.1 times higher at Lake
Waiau than at the sea level site and the ratio of the
short wavelength UVR (UV-B 300320 nm) to PAR is
more than 1.25 times higher. Biologically effective ir-
radiances are listed in Table 1C. Weighted irradiances
measured in air were 27, 9.4 and 6% greater at Lake
Waiau than at sea level at Kaneohe Bay, using the
weighting factors for DNA (Setlow, 1974), diatom in-
hibition by UVR (Cullen et al., 1992) and chloroplast
photo-inhibition (Jones & Kok, 1966) respectively.
The 5-cm of water covering the sensor of the spectro-
radiometer and the incubation experiments provided
a substantial reduction in biologically effective dose.
The attenuation coefficient (Kd m1 ) ranges from over
20 to approximately 6 in the UV portion (300400 nm)
of the spectrum (Figure 2). The greatest reduction ob-
served was 73%, determined using the DNA weighting
function, while the diatom photoinhibition weighting
function indicated a reduction of only 43% below that
27
Figure 2. Spectral attenuation coefficient (Kd , m1 ) of Lake Waiau
water on July 16 1994.
Table 2. Characteristics of water at Lake Waiau on
July 16 1994
Chl a (mg l1 ) 0.031
(water column)
Dissolved organic carbon (mg l1 ) 7.08
Phosphate (PO4 ) (M) 1.87
Nitrate + nitrite (NO3 + NO2 ) (M) 0.0
Ammonium (NH4 ) (M) 0.82
Silicate (Si) (M) 382.9
Dissolved organic phosphorus (M) 1.2
Dissolved organic nitrogen (M) 45.52
Total phosphorus (M) 30.7
Total nitrogen (M) 46.34
reaching the lake surface. Temperature ranged from a
maximum of 12 C at 16:00 to a minimum of 5.5 C
at 06:00 (Figure 3).
The lake phytoplankton consisted of a mixture of
cyanophytes (primarily Anabaena and Oscillatoria),
desmids (Closterium, Cosmarium and Sphaerozonia),
as well as unidentified naviculoid diatoms. Water col-
umn Chl a was 0.031 mg l1 (Table 2). Dissolved
inorganic nitrogen was very low with 98% of water
column nitrogen being in the organic fraction. Dis-
solved inorganic phosphorus was substantially higher
than dissolved inorganic nitrogen. The ratio of total
nitrogen to total phosphorus was only 1.5.
The algal mats were dominated by Gloethece,
Phormidium and Anabaena. Fresh mats were up to
1 cm thick and contained substantial sediment mixed
in with the cyanophyte filaments. The AFDM:DM ra-
28

Figure 3. Water temperature ( C) of Lake Waiau at 5 cm depth from noon July 16 1994 to noon July 17 1994.

Table 3. Mean net oxygen production of two photoautotrophic

communities at Lake Waiau
given in Table 3. UVR effects on the water column
plankton in these incubations appear to be so great
(mg O2 mg Chl a1 h1) that net photosynthesis is negative, and significantly
(P < 0.05 paired t-test) less than the UVO treatment.
Water column phytoplankton
In fact, the average gross oxygen production in the
Dark bottle 8.30
UVR transparent bottles was 4.27 mg O2 mg Chl a
Par only 16.71
Ambient (PAR + UVR) 12.57
h1 indicating that UVR effects on respiration were
greater than the energetic gains associated with photo-
Algal mats synthesis under the experimental conditions. The mats
Dark 0.131 exposed to UVR did show net productivity under UVR
Par only UVO 0.684 exposure, though at a rate of only 54% of the mats pro-
Ambient (PAR + UVR) 0.368 tected from UV. Photosynthesis in the water column
normalized to Chl a under no UVR conditions was
45 times that of the mats exposed to UVR. Reduction
in photosynthetic rate in temperate lakes due to UVR
has been demonstrated (Kim & Watanabe, 1993) but
tio was 0.80 indicating that about 20% of the mat mass in that study, even at the surface, there was positive
was inorganic material. Density of the mats was 8 mg net photosynthesis.
AFDM cm2 . The primary productivity of the wa- MAAs were detected both in the water column
ter column planktonic communities and the mats are phytoplankton and in the benthic mat (Table 4). MAA

Table 4. Concentrations of mycosporine-like amino acids (nmol MAA mg protein1 ) from
Lake Waiau (means 1 standard deviation)
Mycosporine
glycine
Water column 0 0
Algal mat 3.3312.401 21.5585.637
concentration in the mat was two to three orders of
magnitude higher than in the water column. Porphyra-
334 was the dominant MAA in the mats and the only
MAA detected in the water column samples.
Discussion
The Lake Waiau system is clearly influenced by the
UVR levels that are up to 20% higher than at sea
level at a comparable latitude. In the lake, primary
productivity occurs in two communities, which show
different responses to UVR exposure. Water column
algae, when confined to BOD bottles held just be-
low the surface, are not able to photosynthesize under
the ambient UVR conditions that prevail at noon. In
naturally circulating waters phytoplankton cells prob-
ably do not spend extended periods of time in the
uppermost strata where UVR effects are strongest.
Maciolek (1969) stated that Lake Waiau was simi-
lar to cold monomictic lakes and that it was unlikely
to stratify in the summer. When vertical movements
are eliminated by positioning incubation bottles at
the surface, the phytoplankton probably receive un-
naturally high UVR doses. Vertical movement in the
cyanobacterial mats in Lake Waiau was constrained,
unlike mats with motile species such as diatoms which
can avoid harmful levels of UVR (Sundbck et al.,
1997). However, self-shading as well as shading by
included sediment material and a greater water column
length for the deeper mats may confer some protec-
tion. Additionally, species found in mats may have
other means of protection. The presence of a phyto-
plankton assemblage in the lake could be explained
by two non-exclusive hypotheses. First, the algae in
the water column could be meroplanktonic, derived
from benthic algal populations in deeper waters held
in suspension by water movements. The benthic al-
gae could be protected from harmful UVR effects but
the derived meroplanktonic cells might not be photo-
synthetically active when they were brought near the
29
Shinorine Porphyra-334 Palythinol
1.2750.928 0
177.32631.326 1.8681.481
surface. Second, the conditions in the experiment con-
strain the algae to remain at the very surface of the
lake. Because of the generally windy conditions at the
summit of Mauna Kea there is considerable mixing
and the amount of time algae spend very close to the
surface is probably less than in our experiment. Given
the high attenuation of the lake water, primary pro-
ductivity in the water column may be protected from
inhibitory levels of UVR. This important aspect of
water column circulation ameliorating harmful effects
of UVR has been stressed by oceanographers (Cullen
& Lesser, 1991). Specifically, the amount of DOC in
Lake Waiau (Table 2) may be responsible for the large
vertical attenuation coefficient as described for other
lake systems (Williamson et al., 1996). The observa-
tion that Porphyra-334 was the principal MAA in the
mats and the only one detected in the water column
might suggest that at least some of the algae in the
water column are derived from benthic populations.
The presence of only one MAA, Porphyra-334 with an
absorption maximum of 334 nm, in the water column
sample indicates that protection from UVR is princi-
pally restricted to the shorter wavelengths of UV-A
radiation for phytoplankton in this system. Species of
coral and algae which contain several different types
of MAAs, with absorption maxima ranging from UV-
B and into the short wavelength UV-A region of the
spectrum, provide broad-band protection from poten-
tially harmful UV wavelengths (Dunlap et al., 1986).
There was no evidence of other UV-absorbing com-
pounds in either the mat or the plankton samples and,
in particular, no evidence of a 326-nm absorbing com-
pound as found by Garcia-Pichel et al. (1993) in the
cyanobacterium Gloeocapsa sp.
The algal mats do show net oxygen production
even under ambient UVR. These benthic mats are sta-
tionary and are continually exposed to the continuous
UVR irradiance to which they have acclimated over
time. The thickness of the mats probably causes a
high degree of self-shading, which is probably why
the Chl a-adjusted photosynthetic rates in the mats is
30
lower than in the water column phytoplankton. Addi-
tionally, the mats contain high concentrations of the
UVR-blocking MAAs which is consistent with the
idea that they are protected from ambient levels of
UVR. Even so, under UVR-free conditions, the effi-
ciency of photosynthesis in the mats, adjusted for Chl
a is only about 4% of the water column algae.
High UVR irradiance incident on tropical moun-
tain ecosystems (Lee & Lowry, 1980) has a greater
negative effect on photosynthetic aquatic communities
than at lower elevations (Gala & Giesy, 1991; Kim &
Watanabe, 1993). The organisms may achieve some
protection from these effects from their MAAs, but
may also require either strong vertical circulation (for
the planktonic forms) or self- or sediment-shading (for
the mats). Nevertheless this lake supports substantial
amounts of photosynthetic biomass in the mat com-
munity and sometimes in the planktonic phase (Laws
& Woodcock, 1981).
Lake Waiau represents an extreme example of
UVR impact on a natural community, yet this lake
harbors a diverse and productive assemblage of organ-
isms. Lake Waiau is a natural laboratory for the study
of impacts of UVR in natural systems.
Acknowledgments
This work was carried out during the 1994 Hawaii
Institute of Marine Biology Summer Program on Ul-
traviolet Radiation and Coral Reefs. Funding for this
program was provided by the Edwin Pauley Founda-
tion. This work was also supported by the National
Science Foundation (OCE-9216307/OCE-9496082 to
MPL). We thank Dr Isabella Abbott for help in iden-
tifying algal species. MAA standards were made by
W. Dunlap and provided by D. Karentz. Logistic sup-
port was provided by Hawaii Preparatory Academy
Waimea, Hawaii. M. Rice of HPA and D. Gulko of
HIMB assisted with field work.
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