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Hydrobiologia
DOI 10.1007/s10750-010-0147-5
MOUNTAIN LAKES
How do UV radiation, temperature, and zooplankton
influence the dynamics of alpine phytoplankton
communities?
Craig E. Williamson • Courtney Salm
Sandra. L. Cooke • Jasmine. E. Saros
•
Ó Springer Science+Business Media B.V. 2010
Abstract Plankton in mountain lakes are confronted
with generally higher levels of incident ultraviolet
radiation (UVR), lower temperatures, and shorter
growing seasons than their lower elevation counterparts. The direct inhibitory effects of high UVR and
low temperatures on montane phytoplankton are
widely recognized. Yet little is known about the
indirect effects of these two abiotic factors on phytoplankton, and more specifically whether they alter
zooplankton grazing rates which may in turn influence
Guest editors: Hilde Eggermont, Martin Kernan & Koen
Martens / Global change impacts on mountain lakes
C. E. Williamson Sandra. L. Cooke
Department of Earth & Environmental Sciences,
Lehigh University, Bethlehem, PA 18015, USA
C. E. Williamson (&)
Department of Zoology, Miami University, Oxford,
OH 45056, USA
e-mail: [email protected]
C. Salm Jasmine. E. Saros
Department of Biology, University of Wisconsin-La
Crosse, La Crosse, WI, USA
C. Salm Jasmine. E. Saros
Department of Biology & Ecology,
Climate Change Institute, University of Maine,
Orono, ME 04469, USA
Sandra. L. Cooke
Department of Biology, Duke University,
Box 90025, Durham, NC 27708, USA
phytoplankton. Here, we report the results of field
microcosm experiments that examine the impact of
temperature and UVR on phytoplankton growth rates
and zooplankton grazing rates (by adult female
calanoid copepods). We also examine consequent
changes in the absolute and relative abundance of the
four dominant phytoplankton species present in the
source lake (Asterionella formosa, Dinobryon sp.,
Discostella stelligera, and Fragilaria crotonensis). All
four species exhibited higher growth rates at higher
temperatures and three of the four species (all except
Dinobryon) exhibited lower growth rates in the
presence of UVR versus when shielded from UVR.
The in situ grazing rates of zooplankton had significant
effects on all species except Asterionella. Lower
temperatures significantly reduced grazing rates on
Fragilaria and Discostella, but not Dinobryon. While
UVR had no effect on zooplankton grazing on any of
the four species, there was a significant interaction
effect of temperature and UVR on zooplankton
grazing on Dinobryon. Discostella and Dinobryon
increased in abundance relative to the other species in
the presence of UVR. Colder temperatures, the
presence of zooplankton, and UVR all had consistently
negative effects on rates of increase in overall
phytoplankton biomass. These results demonstrate
the importance of indirect as well as direct effects of
climate forcing by UVR and temperature on phytoplankton community composition in mountain lakes,
and suggest that warmer climates and higher UVR
levels may favor certain species over others.
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Hydrobiologia
Keywords Alpine lake Zooplankton grazing Ultraviolet radiation Temperature Climate change Phytoplankton
Introduction
Mountain lakes are some of the most sensitive
indicators of environmental change (Williamson
et al., 2008; Williamson et al., 2009). Their high
elevation leads to increased exposure to ultraviolet
radiation (UVR) as well as a shortened growing season
that aggravates both temperature and light limitation in
plankton populations (Sommaruga, 2001). They are
often remote and therefore some distance from disturbance and nutrient sources. This together with their
characteristically small watersheds increases the
severity of nutrient limitation in these systems. The
importance of light, temperature, and nutrient limitation have been clearly demonstrated in the alpine and
subalpine lakes of the study sites in the Beartooth
Mountains of Montana/Wyoming (Doyle et al., 2005;
Saros et al., 2005a), and we present additional data on
these here. Even small environmental perturbations
can induce detectable changes in community composition and/or ecosystem structure and function in
mountain lakes. For example, there is evidence that
among-year differences in climate lead to decreases in
autotrophic phytoplankton and increases in mixotrophic algal species as well as in species richness in
years with higher winter snowfall, later ice-out, and
dryer summers (Parker et al., 2008). One of the
primary challenges that remain, however, is to clarify
the role of indirect effects of food web responses in this
otherwise largely abiotic forcing. For example, might
responses of zooplankton to climate forcing alter the
community structure of the phytoplankton community
on which they graze?
Based on the sedimentary diatom records, dramatic shifts in phytoplankton community structure
have occurred recently in alpine lakes in many
regions of the world (Arzet, 1987; Psenner &
Schmidt, 1992; Wolfe et al., 2001; Saros et al.,
2003). These changes in diatom species composition
provide valuable signals of past environmental
change. Recent studies in the Rocky Mountains of
the USA have demonstrated that nitrogen deposition
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is responsible for some of these changes (Saros et al.,
2005b).
Temperature and UVR are also likely to play an
important role in regulating these observed changes
in phytoplankton community structure. The ice-free
season when temperatures are warmer, is generally
only a few months long, and even during this period
the warmer parts of the lake are generally limited to
just a few meters depth near the surface of the lake,
where UVR exposure levels are potentially very high.
On the one hand, the well-lit warmer surface waters
offer an opportunity for tremendously enhanced
growth rates for phytoplankton. For example, increasing temperatures from about 6–14°C can increase
growth rates of some diatom species by more than
10-fold (Doyle et al., 2005). Alternatively, phytoplankton growth rates can be inhibited by the UVR
levels experienced in the warmer surface waters
(Doyle et al., 2005), so that the response of phytoplankton and other algae to UVR is complex and
temperature dependent (Rae & Vincent, 1998; Roos
& Vincent, 1998).
The combined roles of UVR radiation and temperature on zooplankton grazing and the consequences for phytoplankton community structure are
less well understood. While several authors have
studied the changes in the nutritional quality of algae
exposed to UVR and the potential consequences for
zooplankton grazers (Wang & Chai, 1994; Van Donk
& Hessen, 1995; Arts & Rai, 1997; Hessen et al.,
1997; Van Donk, 1997; Scott et al., 1999; de Lange &
Lurling, 2003; Leu et al., 2006), to our knowledge
there have been no studies that have examined the
effects of UVR and temperature on zooplankton
grazing rates and the subsequent effects on phytoplankton communities. The major role that zooplankton grazing can play in the development of the deep
chlorophyll maximum in high elevation lakes demonstrates the importance of these trophic interactions
in altering phytoplankton communities (Pilati &
Wurtsbaugh, 2003). UVR may also play an important
role in the development of the deep chlorophyll
maximum in some high elevation lakes (Sommaruga,
2001), but not in others (Saros et al., 2005a). The
potential impact of UVR on invertebrate grazers has
been well demonstrated in other aquatic ecosystems.
For example, in streams, the greater sensitivity of
chironomid grazers to UVR in comparison to their
Hydrobiologia
periphyton food can actually lead to an increase in
periphyton biomass over longer time periods (Bothwell et al., 1993, 1994). Similar effects of decreased
grazing in the presence of UVR have been observed
in marine heterotrophic nanoflagellates feeding on
phytoplankton (Ochs & Eddy, 1998) and terrestrial
insects feeding on plants (Ballaré et al., 2001).
Here we attempt to tease apart the direct and
indirect effects of UVR, temperature, and zooplankton grazing on alpine phytoplankton by incubating
natural phytoplankton communities in the presence
and absence of UVR at two different temperatures in
the presence and absence of zooplankton grazers. We
focus on two major questions. First, how are
zooplankton grazing rates influenced by UVR and
temperature? Second, is the magnitude of the effects
of UVR and temperature on zooplankton grazing
rates large enough to alter phytoplankton population
growth rates and hence community structure under
different UVR and temperature conditions?
Materials and methods
The experimental study sites are located in the
Beartooth Mountains of the Absaroka-Beartooth
Wilderness Area in western Montana and Wyoming,
USA. The experimental design was a 2 9 2 9 2
factorial with four replicates, where the factors were
UVR, temperature, and zooplankton grazers. The
approach involved collecting water and plankton
from a subalpine source lake and incubating them in
microcosms at the surface of the two incubation
sites—one a cool subalpine lake, and the other a
warmer subalpine pond. Within each site microcosms
were either shielded or exposed to natural UVR, and
zooplankton grazers were added to half of the bags.
The source lake for the water and plankton was
Beartooth Lake, a circumneutral (pH *7.3) and
transparent oligotrophic lake (chlorophyll concentration \1 lg l-1, DOC concentration *1.0 mg l-1)
located at an elevation of 2,713 m, 44° 580 N; 109°
340 W. Beartooth Lake, like other lakes in the region,
has a phytoplankton assemblage dominated by diatoms early in the summer as well as later in the icefree season, with often more abundant flagellates
during mid to late July. Ice-out in Beartooth Lake is
generally in mid to late June. The calanoid copepod
Leptodiaptomus ashlandi (Marsh) is the dominant
crustacean zooplankter in Beartooth Lake in June and
July following ice-out, with densities that reach four
to five individuals per liter. In other nearby subalpine
lakes L. ashlandi may reach peak densities in excess
of 30 per liter. Calanoid copepods generally dominate
early in the year in most of the alpine and subalpine
lakes in the region, giving way to cladoceran
populations, and Daphnia pulex in particular, as the
lakes warm up in late July and August. Rotifers are
generally present at only low densities. Our prior
experiments have demonstrated that adult female
L. ashlandi are quite UVR tolerant and not likely to
perish at the exposure levels used in these experiments (Cooke et al., 2006). We focused on the
sublethal effects of UVR and temperature on grazing
rates of L. ashlandi.
Whole lake water containing natural phytoplankton
communities was collected from a depth of 7 m (depth
of the chlorophyll maximum) in Beartooth Lake and
used as the incubation water. The L. ashlandi were
collected the day before the experiment with a vertical
tow of a 30-cm diameter 243-lm mesh plankton net.
The copepods were isolated into small dishes and kept
at lake temperature in a dark cooler overnight. On the
day of the experiment, six adult females with eggs
were added to 750 ml of lake water in each replicate
20 9 18 9 5 cm polyethylene (Bitran) bag. Before
addition of lake water, 30% of the volume was filtered
through a 1-lm pre-filter and 0.2-lm filter (hydrophilic polymer filters) using a canister filtration
apparatus with polypropylene and ultra-high density
polyethylene screen retainers (Cole-Palmer and
Corning). This reduced the food densities somewhat
below ambient to permit comparison with a parallel
experiment on the effects of UVR and dissolved organic
matter on zooplankton survival (Cooke et al., 2006).
The microcosms were suspended horizontally at
the very surface of the incubation lakes in racks and
covered with window screen mesh bags that acted as
neutral density filters to reduce incident sunlight by
62%. Eight of these bags were further shielded from
UVR by covering them with Courtgard, while the
other eight were covered with Aclar, a UVR-transparent plastic. Courtgard is a long-wave-pass plastic
that transmits PAR (95% 400–800 nm in water) but
blocks most UVR (transmits no UV-B 295–319 nm,
and only 9% of UV-A 320–400 nm with a sharp
wavelength cutoff and 50% transmittance at 400 nm).
Aclar is a long-wave-pass plastic that in water
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transmits both PAR (100% 400–800 nm) and most
UVR (98% of UV-B 295–319 nm, 99% UV-A 320–
399 nm, with a sharp wavelength cutoff and 50%
transmittance at 212 nm).
On 2 July 2004 the microcosms were deployed in
Beauty Lake at 11:00 MT and in Meadow Pond #2 at
14:30 MT. Nutrients (18 lmol l-1 of nitrogen as
NaNO3 and 5 lmol l-1 of phosphorus as NaH2PO4H2O) were added to all microcosms to alleviate
the potential for differences in phytoplankton growth
rates due to nutrient additions from zooplankton
excretion in the microcosms with zooplankton.
Nutrient concentrations in Beartooth Lake at the
time of the incubations were 3.66 lM of N and
0.08 lM of P. The experiment was taken down on 9
July 2004 by removing the microcosms from Beauty
Lake at 13:40 MT and from Meadow Pond #2 at
17:30 MT, mixing the microcosms by inverting them
several times, and preserving 50-ml subsamples with
Lugol’s iodine.
Temperature in both incubation lakes was measured with iButton thermocron DS1921 programmable temperature loggers (Maxim Dallas Direct,
Dallas, TX, USA) attached below the protective
plastics (2 Aclar, 2 Courtgard). Solar radiation data
were collected with an internally logging BIC
radiometer (Biospherical Instruments Inc., San
Diego, CA, USA) deployed on top of a nearby
observation tower on Clay Butte (44° 570 N, 109°
370 W) at an elevation of 3,175 m. This instrument is
a medium-bandwidth instrument (8–10 nm full width
at half maximum for the UVR channels) that records
incident UVR irradiance at 305, 320, and 380 nm, as
well as PAR (400–700 nm). Incident UVR levels are
reported for the 320 nm wavelength band. These
wavelengths are the most biologically relevant when
considering the spectral composition of incident UVR
and the photon-specific damage of UVR on plankton
(Williamson et al., 2001).
Phytoplankton communities were quantified by
enumeration on an inverted microscope in the
laboratory. Samples were settled in Utermöhl-style
chambers and counted with an inverted microscope
(Nikon TS-100) at 4009 magnification. Four transects were counted for each sample, with additional
transects added as needed so that at least 500
individuals were counted. Taxonomy was based on
standard references (Krammer & Lange-Bertalot,
1986–1991; Wehr & Sheath, 2003). Phytoplankton
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biovolumes were estimated by measuring the dimensions of 20 individuals of each species and using the
relevant geometric shape.
Phytoplankton growth rates and zooplankton grazing rates were estimated with an exponential model
using instantaneous rates of change estimated from ln
(Nt/No), where N0 and Nt were the starting and final
densities of each species. Phytoplankton growth rates
(b) were estimated by using the final phytoplankton
density in the absence of zooplankton for Nt.
Instantaneous rates of increase of phytoplankton
population density (r) were estimated by using the
final phytoplankton density in the presence of zooplankton for Nt. Instantaneous grazing rates (d) were
then estimated as the difference (d = b - r). The
standard errors for d were calculated as the square
root of the sum of each of the individual standard
errors squared for b and r. All rates are expressed for
the duration of the experiment (per week) and the
grazing rates are per six adult female copepods (plus
the 5–10 nauplii per female produced during the
incubation) per week.
A three-way analysis of variance (ANOVA) with
temperature, UVR, and zooplankton as the three
factors was carried out on the raw phytoplankton
counts to test for the significance of temperature
effects on phytoplankton growth rates (temperature
effect), UVR effects on phytoplankton growth rates
(UVR effects), zooplankton grazing rates (zooplankton effect), as well as the effects of temperature and
UVR alone and together on zooplankton grazing rates
(temperature–zooplankton, UVR–zooplankton, and
UVR–temperature–zooplankton interaction effects,
respectively).
Results
The weather throughout the 7-day experimental
period was largely clear and cloudless with afternoon
thunderstorms on 4 of the 7 days. Mean exposure
temperatures in the microcosms in the cooler and
warmer treatments were 8.3°C (range of 6.5–10.0°C)
and 11.7°C (range of 7.5–16.0°C), respectively.
Cumulative incident UVR exposure levels over the
7-day experimental period were 54.1 kJ m-2 for the
320-nm waveband of the BIC logger. The combination of albedo at the surface of the lake, and reduction
in UVR transmission due to the mesh screen, Aclar,
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throughout the Beartooth Mountains. Additional taxa
present in the lake included the diatoms Aulacoseira
alpigena (Grunow) and Krammer, and A. distans
Ehrenberg, and the dinoflagellate Gymnodinium. As
these taxa made up a smaller portion of the total
biovolumes for final treatment assemblages (Aulacoseira species averaging less than 1% each and
Gymnodinium averaging less than 15%), our analyses
focused on changes in the four dominant phytoplankton taxa that are commonly found across the region.
Higher temperatures significantly enhanced the
growth rates of all four major phytoplankton taxa
(Table 1). Fragilaria and Discostella showed the
strongest response to temperature (Fig. 1). The presence
of UVR significantly decreased the growth rates of
Fragilaria, Asterionella, and Discostella, but not Dinobryon (Table 1; Fig. 1). Interestingly, the response of
Dinobryon, though not significant, was an increase in
and the water transparency in the bags brought the
cumulative UVR exposure levels in the middle of
these bags down to 29.1 kJ m-2 at 320 nm in the
UVR? treatments. DNA dosimeters that measure
potential UVR damage demonstrated the strong
differences in the UVR exposure in the treatments
that were shielded versus un-shielded from UVR;
these data are presented elsewhere (Cooke et al.,
2006).
The phytoplankton assemblage of Beartooth Lake
was primarily dominated by diatoms, including
Fragilaria crotonensis Kitton, Asterionella formosa
Hassall, and Discostella stelligera Houk and Klee,
and a chrysophyte, Dinobryon, hereafter referred to
by their genera names to facilitate discussion. These
taxa were dominant across all experimental treatments, and are representative of phytoplankton
assemblages found in alpine and subalpine lakes
Table 1 Results of threeway ANOVA where
zooplankton (presence vs.
absence), UVR (presence
vs. absence) and
temperature (8.3 vs. 11.7°C)
were the three factors
Bold values represent
statistically significant
effects (P \ 0.05)
Treatment
Dinobryon
Temp
<0.001
UVR
0.589
Zoop
Fragilaria
Asterionella
Discostella
<0.001
<0.001
<0.001
<0.001
<0.001
0.046
0.004
<0.001
<0.001
0.066
UVR*Temp
0.254
0.091
0.986
0.142
Zoop*Temp
0.198
0.002
0.442
0.004
Zoop*UVR
0.087
0.447
0.543
0.696
Zoop*UVR*Temp
0.019
0.914
0.078
0.564
Fig. 1 Phytoplankton
exponential growth rates
(population change per
week) at cool (C, 8.3°C
average) and warm (W,
11.7°C average)
temperatures in the
presence (UVR?) and
absence (UVR-) of UVR
for the four dominant
phytoplankton species
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growth rate in the presence of UVR in the warmer
treatments. There were no significant interactive effects
of UVR and temperature on the growth rates of any
species (Table 1).
Zooplankton grazing led to significant decreases in
Dinobryon, Fragilaria, and Discostella, but not
Asterionella (Table 1; Fig. 2). Grazing rates were
significantly higher at the higher temperatures only
for Fragilaria and Discostella; with the highest
grazing rates observed on Discostella at the higher
temperatures (Fig. 2). Although grazing rates tended
to be higher in the presence of UVR (Fig. 2), there
were no significant effects of UVR on the grazing
rates on any of the four species. UVR and temperature had a significant interactive effect on grazing on
Dinobryon (Table 1), with substantially lower grazing rates in the warm treatment with no UVR
compared to the other three treatments (Fig. 2).
The combined effects of temperature, UVR, and
zooplankton grazing led to several pronounced
changes in the absolute and relative abundance of
the four dominant species and thus phytoplankton
community structure. In all treatments the total
phytoplankton biovolume increased in comparison
to the initial levels over the experimental period
(Fig. 3A). Total phytoplankton biovolume also consistently increased in response to warmer temperatures, and consistently decreased in response to both
UVR and zooplankton grazers (Fig. 3A), suggesting
Fig. 2 Zooplankton
exponential grazing rates
(per six copepods and their
nauplii per week) on
phytoplankton at cool (C,
8.3°C average) and warm
(W, 11.7°C average)
temperatures in the
presence (UVR?) and
absence (UVR-) of UVR
for the four dominant
phytoplankton species
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the lack of any strong compensatory responses among
species. There were, however, shifts in the relative
abundance of phytoplankton species during the
experiment. The relative abundance of Asterionella
increased, while the relative abundance of Fragilaria
decreased across all treatments (Fig. 3B). The final
relative abundance of Fragilaria was generally
greater at higher temperatures than it was at the
lower temperatures regardless of the presence or
absence of UVR or zooplankton grazers (Fig. 3B),
consistent with the strong temperature dependent
growth rate responses in this species (Fig. 1). While
Discostella exhibited a similar strong response to
temperature (Fig. 1), the much higher grazing rates at
higher temperatures on this species (Fig. 2) offset the
higher growth rates in the presence of zooplankton
(Fig. 3B). At the higher temperature the relative
abundance of Asterionella was greater in the presence
of zooplankton (Fig. 3B), which is consistent with the
generally higher grazing rates on the other species at
the higher temperatures (Fig. 2). These patterns did
not hold at the lower temperatures. Zooplankton
grazing resulted in a decrease in the relative abundance of Discostella and an increase in the relative
abundance of Asterionella at higher temperatures, but
not at lower temperatures (Fig. 3).
Two species actually did better relative to the other
species in the presence of UVR. The relative
abundance of Dinobryon was approximately twice
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Fig. 3 Absolute (A) and relative (B) abundance (biovolume) of
the four major phytoplankton taxa (Aster = Asterionella,
Disco = Discostella, Dinob = Dinobryon, and Fragil = Fragilaria) at the start (initial) and end (all other bars) of the
experiment in the presence and absence of zooplankton (Z) in
warm (W, 11.7°C average) and cool (C, 8.3°C average)
treatments with and without UV radiation
as high in the presence of UVR versus in its absence
across all temperature and zooplankton treatments
(Fig. 3B). Discostella also was relatively more
abundant in the presence of UVR than in its absence,
but only at the lower temperatures. This effect was
particularly apparent for Discostella in the absence of
zooplankton grazers (Fig. 3B). Dinobryon was also
relatively more abundant at lower versus higher
temperatures across all treatments (Fig. 3B). This is
consistent with the observation that although Dinobryon, like all species, exhibited higher growth rates
at higher temperatures (Table 1), its growth rate
response to temperature was less pronounced in
comparison to the other three species (Fig. 1).
Discussion
While strong effects of temperature and UVR were
apparent on phytoplankton growth rates in our
experiments (Table 1), their effects on zooplankton
grazing were less pronounced. There were positive
synergistic effects of temperature and zooplankton
grazing on Discostella and Fragilaria as evidenced
by the interactive effects of temperature and zooplankton on these two species (Table 1; Fig. 2). The
lack of any interactive effects of UVR and zooplankton on phytoplankton responses (Table 1) indicates
that UVR did not influence zooplankton grazing.
However, the effects of UVR on the reproduction of
the copepods reported previously in these experiments (Cooke et al., 2006) suggest that the longer
term responses of plankton communities to UVR may
be altered by changes in zooplankton population sizes
as well as the direct response of phytoplankton to
UVR and grazing. The time scale of our experiments
was not adequate to take into account such numerical
responses in the zooplankton populations.
The consequences of the combined effects of UVR
and temperature on zooplankton grazing for phytoplankton community structure were most evident at
the higher temperatures. They included a greater
relative abundance of Asterionella in the presence of
zooplankton and a greater relative abundance of
Discostella in the absence of zooplankton (Fig. 3). In
addition, at lower temperatures Discostella did better
relative to other species in the presence of UVR than
in its absence (Fig. 3), though this change in relative
abundance was due more to a reduced sensitivity of
Discostella to UVR at these lower temperatures and
not greater growth rates in the presence of UVR
(Fig. 1). While there is evidence that nitrogen
deposition may be the strongest driver of diatom
changes in these lakes (Saros et al., 2005b), our
research suggests that the indirect effects of UVR and
temperature on trophic interactions may also contribute, in part, to recent patterns of change in phytoplankton community structure. Unfortunately, no data
are available from past sediment samples on how
zooplankton communities have changed in recent
years. What is apparent is that zooplankton grazing is
a potentially important variable to consider when
looking at the impact of abiotic factors on changes in
phytoplankton community structure in either neoecological or paleoecological studies.
The effects of UVR and temperature on growth
rates of Asterionella, Dinobryon, and Fragilaria are
generally consistent with those reported previously
(Doyle et al., 2005) with the exception that in the
current experiment the growth response of Dinobryon
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to UVR was not significant, and there were no
interactive effects of UVR and temperature on the
growth rates of any of these three species (Table 1).
These differences between experiments may be due
to the reduced temperature range used here (8.3–
11.7°C) in comparison to that used by Doyle et al.
(2005) (6.1–14.0°C).
The higher grazing rates that we observed on the
unicellular diatom Discostella compared to the other
three colonial species is consistent with previous
experiments that have demonstrated higher grazing
rates by Daphnia on a similarly-sized unicellular
diatom Stephanodiscus hantzschii relative to a suite
of colonial diatoms including A. formosa, F. crotonensis, Tabellaria fenestrata, and Melosira italica
(Infante & Litt, 1985).
There are other possible mechanisms by which
UVR can influence grazing rates of zooplankton. For
example, exposure to UVR may reduce the nutritional quality of phytoplankton for zooplankton
(references in introduction). Sublethal exposure to
UV-B also leads to an increase in cell size in diatoms
and other algae due to decoupling of the accumulation of fixed carbon from photosynthesis and a
decrease in cell division rates (Hessen et al., 1997).
Changes in cell sizes have the potential to alter sizeselective feeding in zooplankton. The generally
greater response of the phytoplankton in this study
to UVR and temperature in comparison to the
zooplankton grazers may also be related to the fact
that the phytoplankton were collected from deeper
waters with lower temperature and UVR while the
zooplankton were collected with vertical tows, and
some portion of the zooplankton may thus have been
more acclimated to the warmer, higher UVR and
temperatures in the surface waters.
Conclusion
Temperature, UVR, and zooplankton grazing can all
alter the in situ growth rates of phytoplankton in
montane lakes. It is important to realize that these
changes were observed in the presence of nutrient
additions. While there is good evidence that nutrients
are increasing in many alpine regions including the
Beartooth Mountains (Sickman et al., 2003, Saros
et al., 2005b), the synergistic effects of nutrients and
these other variables may vary with species and
123
region. Whether these patterns apply to regions where
nutrients are not increasing is not known. The
ultimate impact of variations in UVR and temperature on phytoplankton communities is likely to be a
function of many factors. This includes the relative
UVR sensitivity and temperature dependence of not
only phytoplankton growth rates, but also zooplankton grazing rates. These grazing rates may also be
influenced by the effects of temperature and UV on
the vertical and seasonal overlap of zooplankton and
phytoplankton and the potential for either seasonal
mismatches between zooplankton grazers and phytoplankton (Winder & Schindler, 2004), or alteration of
vertical overlap with food resources (Leech &
Williamson, 2001, Cooke et al., 2008) or predators
(Williamson et al., 1999, Boeing et al., 2004). The
timing of changes in UVR exposure levels and
acclimation responses may also be important in
determining the ultimate impacts of UVR on algae
(Roos & Vincent, 1998).
Acknowledgments We thank Ryan Lockwood, Kirsten
Kessler, Lindsay Boateng, Shaina Keseley, and Caren Scott
for field assistance. This work was supported by NSF Grant
DEB-IRCEB-0210972.
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Figure 2
2.5
Grazing Rate
2.0
1.5
1.0
0.5
0.0
-0.5
2.5
Grazing Rate
Fragilaria
Dinobryon
CUV+
CUV-
WUV+
WUV-
1.5
1.0
0.5
0.0
Asterionella
CUV+
CUV-
WUV+ WUV-
Discostella
2.5
2.0
1.5
1.0
0.5
0.0
-0.5
2.0
-0.5
Grazing Rate
Grazing Rate
2.5
CUV+
CUV-
WUV+
WUV-
2.0
1.5
1.0
0.5
0.0
-0.5
CUV+
CUV-
WUV+ WUV-