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Journal of Plankton Research Vol.9 no.2 pp.327-344, 1987
Summer dynamics of the deep chlorophyll maximum in
Lake Tahoe
Thomas G.Coon, Matilde Lopez M. 1 , Peter J. Richerson2, Thomas
M.Powell2 and Charles R.Goldman2
School of Forestry, Fisheries and Wildlife, 112 Stephens Hall, University of
Missouri, Columbia, MO 65211, USA, 1lnstituto de Investigaciones
Oceanologicas, Universidad de Chile, Casilla 1240, Antofagasta, Chile, and
2
Division of Environmental Studies, University of California, Davis, CA
95616, USA
Introduction
A subsurface maximum of chlorophyll concentration has been reported from a variety
of locations in oceans (e.g. Steele and Yentsch, 1960; Anderson, 1969; Venrick etal.,
1973; Beers et al., 1975; Kiefer et al., 1976; Ortner et al., 1980; Cullen and Eppley,
1981; Estrada, 1985) and lakes (e.g. Kiefer etal., 1972; Fee, 1976; Brooks and Torke,
1977; Moll and Stoermer, 1982; Priscu and Goldman, 1983). These features occur
most commonly in stratified systems of low or moderate productivity where the euphotic
zone extends below the mixed layer. They typically occur deep, near the compensation
depth.
In lakes, conspicuous chlorophyll maxima usually occur within or directly below the
thermocline and are associated with a sharp gradient in nutrient concentrations (e.g.
a nitracline) (Ichimura et al., 1968; Kerekes, 1974; Fee, 1976; Brooks and Torke, 1977;
Priscu and Goldman, 1983). However, Lake Tahoe has a distinct deep chlorophyll maximum (DCM) well below the thermocline (Kiefer et al., 1972; Holm-Hansen et al.,
1976; Richerson et al., 1978) that resembles those of seasonally variable, oligotrophic
ocean regions (Cullen, 1982; Abbott et al., 1984; Estrada, 1985) more than those
reported from other lakes.
A subsurface maximum of chlorophyll could result from one or a combination of
three conditions: (i) a maximum of phytoplankton biomass; (ii) a maximum of
chlorophyll concentration per unit cell biomass; or (iii) a maximum of extracellular
chlorophyll.
Venrick etal. (1973), Fee (1976), Richerson etal. (1978), Cullen (1982), and Moll
327
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Abstract. Vertical profiles of chlorophyll and phytoplankton biomass were measured in Lake Tahoe from
July 1976 through April 1977. A deep chlorophyll maximum (DCM) persisted during summer and early
autumn (July-October) near 100 m, well below the mixed layer and at the upper surface of the nitracline.
The DCM coincided with the phytoplankton biomass maximum as determined from cell counts. In addition,
the composition of the phytoplankton assemblage was highly differentiated with respect to depth. Cyclotella
stelligera was the predominant species in the mixed layer while the major species in the DCM layer included
C. ocellata and several green ultraplanktonic species. In situ cell growth plays a substantial role in maintaining the DCM, but sinking of cells from shallower depths and zooplankton grazing above the DCM may
contribute to the maintenance of the DCM. Calculations support the interpretation that the summer DCM
persists at the boundary between an upper, nutrient-limited phytoplankton assemblage and a deeper, lightlimited assemblage.
T.G.Coon et al.
Methods
Fifteen chlorophyll and phytoplankton profiles were collected over a 10-month period
at a station 3 km off Homewood, California. The in vivo fluorescence method (Lorenzen,
1966) was used to sample the chlorophyll profile continuously. Water was drawn through
a 140-m opaque hose (15.8 mm i.d.) by a 1/4-hp electric deck pump at a rate of 5 1
min" 1 . The water was passed through a Turner Designs Model 10 fluorometer on deck,
from which fluorescence was recorded on a Hewlett-Packard chart recorder. For each
profile the hose intake was lowered slowly (10 m min" 1 ) to 140 m to obtain a smooth
in vivo profile and then was raised in 10-m increments, stopping at each depth for 2—3
min to draw an unmixed sample from the hose. These samples were used for the determination of extracted chlorophyll concentration and for cell enumeration.
Samples for pigment extraction were filtered onto Whatman GF/C filters, ground
in a tissue grinder and extracted with 90% acetone. Fluorescence of the extract was
328
and Stoermer (1982) have reviewed hypotheses on the mechanisms by which these conditions might be established and maintained. For chlorophyll maxima which represent
biomass maxima, cells may accumulate by (i) sinking from overlying water and/or (ii)
phytoplankton growth rates which are greater in the maximum region than in shallower
and deeper strata. Such differential growth rates could exist because the maximum region
favors high cell production rates due to high nutrient concentrations (e.g. Moll et al.,
1984) and/or because loss rates (grazing, respiration or cell death) are relatively low
mere (e.g. Fee, 1976). High concentrations of chlorophyll per unit biomass have been
shown to represent a physiological response to low light levels (Jorgensen, 1969; Bannister and Laws, 1980), or a nutrient gradient (Yentsch, 1965; Goldman, 1980). Changes
in species composition may be associated with low C:Chl ratios in the DCM (Jorgensen,
1969; Chan, 1980; Vincent, 1982). Extracellular chlorophyll can usually be discounted
because it is rapidly photo-oxidized (Daley and Brown, 1973).
While DCM phenomena have been described from a variety of lake and oceanic conditions, most discussions of the mechanisms responsible for DCM do not distinguish
between mechanisms of formation and mechanisms of maintenance. With few exceptions (e.g. Fahnenstiel and Glime, 1983; Priscu and Goldman, 1983; Abbott et al.,
1984), the mechanisms by which DCM develop are assumed to maintain the DCM after
it has formed. Yet seasonal changes in light, temperature, turbulence, nutrient and productivity distributions minimize the likelihood that the mechanism of DCM dynamics
are invariant. For these reasons, this study focuses on the dynamics of the Lake Tahoe
DCM after its formation. The processes by which the Lake Tahoe DCM is formed
in spring and early summer are reported by Abbott et al. (1984).
The objectives of this study were to describe: (i) the vertical structure of chlorophyll
in Lake Tahoe relative to physical characteristics of the water column following the
formation of the DCM in 1976 and continuing through the erosion of the DCM in autumn
and winter; (ii) the vertical structure of the phytoplankton community as compared with
the chlorophyll distribution; and (iii) the dynamics of the chlorophyll and phytoplankton
profiles during summer months. Based on this information we assess the above
hypotheses as explanations of the mechanisms by which the Lake Tahoe maximum is
maintained once it has formed.
Tahoe deep chlorophyll dynamics
Results
A DCM was present in Lake Tahoe at a depth of 90-110 m July-October 1976 (Figure
1). Surface concentrations of (acid-corrected) chlorophyll a ranged from 0.11 to 0.22 mg
m~ 3 , whereas the concentrations in the deep maximum ranged from 0.59 to 0.88 mg
m~ J . Phaeopigment concentrations were less than 0.10 mg m~ 3 in the upper 60 m of
water, increasing to a maximum concentration at the same depth as the chlorophyll
maximum (never >0.28 mg m~ 3 ).
The summer chlorophyll maximum was 60—80 m below the mixed layer, at the upper
surface of the nitracline, and between the depths of 1 % and 0.1 % surface irradiance
(Figure 2). On five occasions small secondary chlorophyll peaks occurred in the thermocline near the depth of maximum primary production. Thermocline concentrations never
exceeded 0.35 mg m~ 3 .
In vivo fluorescence profiles closely matched the extracted chlorophyll profiles, so
only the latter are presented in Figure 1. Correlation coefficients for in vivo fluorescence
and extracted chlorophyll ranged from 0.73 to 0.99 on individual profiles, all of which
were highly significant (P < 0.001; Coon, 1978). Particles equal in size to the
ultraplanktonic species may pass through the GF/C filters used for filtering extracted
chlorophyll samples, however the close correlation between in vivo and extracted profiles indicates that the extracted profiles are representative of the chlorophyll depth
distribution. Thus, the only effect of filter passage, if it occurred, would have been
329
measured before and after the addition of HC1 to determine total chlorophyll and
phaeophytin concentrations (Strickland and Parsons, 1972). To calibrate the extracted
fluorescence measurements, a large volume sample (8 — 10 1) was filtered and extracted
as described previously. The concentration of chlorophyll and phaeophytin in this sample
was determined by spectrophotometry, using the equations of Lorenzen (1967).
One liter samples of lake water were filtered through an 80-jtm net to remove
zooplankton and were preserved with 10% formalin for phytoplankton enumeration.
The cells were allowed to settle in the bottles for at least 60 days, after which the upper
800 ml of water was carefully aspirated. The sample was resuspended in the remaining 200 ml. A 50-ml subsample was settled for 20 days and counted at 1000 x magnification on a Wild inverted microscope. These long settling times were necessary to recover
several extremely small but abundant species. One hundred microscope fields distributed
randomly across the bottom of the settling chamber constituted the final subsample.
Cell volume was estimated by measuring the linear dimensions of a large sample of
cells of each species and then calculating the volume of a simple geometric shape approximating the shape of the cell. Phytoplankton biomass was estimated as cell carbon
by using the carbon-cell volume regression equation of Mullin et al. (1966).
Vertical profiles of nitrate-nitrogen, 14C primary production, light penetration and
temperature were obtained as part of the regular monitoring program of the Tahoe
Research Group at a station within 2 km of the chlorophyll sampling station (Goldman,
1981). The TRG profiles included the DCM, but were not as deep as the chlorophyll/
biomass profiles (115 m versus 140 m). Solar irradiance (X = 360-2000 m~ 9 ; not
corrected for PAR) was measured and recorded continuously with a pyrheliometer north
of the chlorophyll sampling station on the west shore of the lake.
T.G.Coon et ai.
CHLOROPHYLL a ( m g m - > )
1040• 0• 0-
1OO110140-
LLJ
o
40-
•o•o1OO-
14O10
30
10
10
10
»
0
O
10
10 O
IP
ID ,
10 O
10
10
BiOMASS ( mg C n v J )
Fig. 1. Vertical profiles of extracted chlorophyll concentration (open squares = Q and phytoplankton biomass
(closed circles •• B). Arrows indicate the depth of the DCM as predicted by the calculations described in the text.
TEMPERATURE <°C)
0
10
20
0
10
10
0
10
tO
0
10
tO
0
10
«o•0
100
\
no
0.1*
_
l0
140
0
10
40 0
10
40 0
10
4O 0
10
4O 0
10
40 O
10
4O 0
0
10
10 0
10
10 O
10
10 0
10
10 0
10
10 0
10
10
10
4O
10
40
1040•0•O\
1001tO14010
4O0
1O
40 0
10
4OO
10
400
10
400
NTTRATE-fflTROGEN ( mg m"1 )
Fig. 2. Vertical profiles of temperature (solid line « T) and nitrate-nitrogen concentrations (open circles
= N). Horizontal bars indicate the depth of 10%, 1% and 0.156 surface irradiance.
330
1M-
Taboe deep chlorophyll dynamics
PRIMARY PRODUCTIVITY (mg C m ^ d y 1 )
104O•O-
U
100
HOMO-
1 JU.76
IS JUL 76
17 SEP 76
24 SEP 76
8 AIM 7S
23 AIM 76
10 SEP 76
eo
•o
100.
110
14O
9 OCT 78 I 22 NOV 76
27 JAN 77
Fig. 3. Vertical profiles of daily l4 C primary production.
331
to yield underestimates of actual chlorophyll concentrations uniformly over all depths.
The in vivo profiles showed some small-scale structure not detected with the 10-m intervals used for the extracted profiles, however sharp layers like those recorded by Fee
(1976) from smaller, more stably stratified lakes were never observed.
Estimates of phytoplankton biomass and extracted chlorophyll from the same depth
were strongly correlated, especially during July and August, when the DCM was most
pronounced (Figure 1). Correlation coefficients between biomass and chlorophyll were
significantly different from zero for each profile (P <0.001) and ranged from 0.87
in July to 0.22 in winter months when little vertical structure existed (correlations are
bound to be dominated by error variance when there is little real variation as in the
winter samples). A deep biomass maximum was always present when a DCM was present, occurring at the same depth as the DCM.
Carbonrchlorophyll ratios (C:Chl) showed no regular relationship to depth, ranging
from 3 to 92 over all depths and all sample dates. The mean integrated C:Chl (16.2)
for the upper 30 m of the water column from July through September was not significantly different (date-paired / = 0.496, d.f. =7,P >0.50) from the mean integrated C:Chl
(17.6) for the 40 m of the water column centered around the DCM. Cullen (1982) found
that the C:Chl ratio is —25 in DCM layers formed as a physiological adaptation to
low light and that the ratio is in the range 150—250 in the surface water of these systems.
The DCM ratios in Lake Tahoe agree closely with Cullen's values, but the surface
estimates are much less than Cullen's. Our method of estimating cell biomass differed
from Cullen's only in the volume-carbon regression equations used (Cullen used the
Strathmann equations; Cullen, 1982), which is not likely to introduce a depth-dependent
bias. Furthermore, the Mullin et al. (1966) method of estimating cell carbon yields
higher carbon values (and therefore higher C:Chl ratios) for diatoms than the Strathmann
T.G.Coon et ai.
(day 1 )
P/B
0
4
0
4
0
4
0
4
0
4
0
4
0
104O •O M1OO110-
• 0-
110-
22 MOV 76 I 27 JAN 77
Fig. 4. Vertical profiles of daily primary production to phytoplankton biomass (P/B) ratios.
equations. Thus it is doubtful that the low C:Chl ratios and the lack of a C:Chl gradient
with depth were due to differences between Cullen's and our methodologies.
The DCM was 60—90 m below the depth of maximum 14C uptake (Zp), which was
at 20 — 30 m for most of the summer (Figure 3). The Zp was deeper in spring (40 m
on 21 April 1977) and early summer (60 m on 2 July 1976); however even on these
dates the biomass and chlorophyll maxima were well below Zp. Carbon uptake was
detected as deep as 120 m (the deepest point where it was measured), indicating that
cells in the DCM were photosynthetically active. Even so, the rate of carbon uptake
was slower in the DCM region than at any depth above the DCM in all but two profiles.
On most dates, the primary productivity to biomass ratio (P/B) was greatest near
the 14C uptake maximum (range = 0.38-7.34 day" 1 ; Figure 4). The P/B values in
the region of the DCM were much lower (range = 0.03—0.13 day" 1 ), especially during
the midsummer period when the maximum was most strongly developed.
Total chlorophyll concentration and total phytoplankton biomass integrated over the
upper 140 m tracked the general trend of surface irradiance throughout much of the
study period (Figure 5). A linear regression of total chlorophyll (TCL) on surface irradiance (TR) was significant (r2 = 0.41, P <0.05). Nitrate values integrated over
the upper 115 m (TNO) also accounted for some of the variation in TCL: a multiple
regression of TCL on 1R and TNO yielded a better fit (r2 = 0.72, P < 0.001) than
the T C L - I R regression. Changes in the region of the DCM made a disproportionate
contribution to the variation in both integrated chlorophyll and integrated nitrate values.
The chlorophyll and biomass profiles represented three different sets of conditions
over the time of the study. During July-September (summer), the lake was stratified
and the DCM/biomass maximum was strongly developed near the compensation depth,
332
• 01OO-
800'
800-
o
<
5 200-0.3 3.
i
Chlorophyll •
-20
JUL
AUG
SEP OCT
1976
NOV
DEC
JAN
FEB MAR
APR
1977
Fig. 5. Time scries of integrated water column chlorophyll content, phytoplankton biomass, nitrate-nitrogen
and solar irradiance at the lake surface. Irradiance values are expressed as three-day means.
well below the thermocline and Zp. The shape of the chlorophyll and biomass profiles, the position of the DCM and the total chlorophyll and total biomass content
of the water column varied over time scales of 7 days or less during this period.
We recorded diel series of vertical profiles on two occasions and found that the position of the DCM did not change on this smaller time scale (Coon, 1978). The most
noteworthy changes were a decline in chlorophyll concentration and in phytoplankton
biomass during a stormy period in early August, followed by an increase in both
parameters from 17 August to 10 September (Figure 5). The chlorophyll and biomass
increases during late August and early September were associated with a shoaling of
the DCM (from 110 to 90 m; Figure 1) and the nitracline (from 120 to 80 m; Figure
2). In spite of these temporal changes in the chlorophyll profiles, on any particular
day, the profiles were similar between stations along cross-lake transects (Coon, 1978).
333
Blonuss
T.G.Coon et al.
From late September to January (autumn-winter), the thermocline deepened and
finally disappeared. Over the same period, the DCM/biomass maximum eroded and
total chlorophyll and biomass concentrations decreased, although the DCM was weakly evident in November, when a temperature gradient was still present at 40 m. Under
isothermal conditions in January, the DCM was absent.
The April (spring) measurements differed from other profiles in that the chlorophyll
and biomass maxima were shallower, while the depth of maximum primary produci i
i i
i i i
i
JUL
AUG
SEP
OCT
NOV
DEC
JAN
FEB
MAR
APR
Cyclotalla ocaUata
AIM
334
8EP
OCT
NOV
DEC
JAN
FEB
MAR
APR
CydoUDa •t*nia«ra
Tafaoe deep chlorophyll dynamics
FEB
MAR
APR
1977
Fig. 6. Time-depth distributions of selected phytoplankton species: (a) CyctoteUa stelligera; (b) C. ocellasa;
(c) Oocystis lacustris; (A) Friedmannia sp. Densities are expressed as 10* I" 1 . Vertical marks on the upper
abscissa indicate sampling dates.
tivity was deeper. This profile was the only one in which the biomass and chlorophyll
peaks were near Zp. Abbott et al. (1984) observed a similar coincidence of maxima
for March-April of 1980.
During summer conditions, the phytoplankton assemblage was strongly differentiated
335
T.G.Coon et at.
with respect to depth. The epilimnion was dominated by the small diatom Cyclotella
stelligera (cell volume = 30.5 /im3, Figure 6a). The DCM was dominated by the larger
C. ocellata (416.3 fim3, Figure 6b). The dominant alga in the middle depths (i.e. between the thermocline and the DCM: 4 0 - 7 0 m) was Oocystis lacustris (160.9 /*m3,
Figure 6c). A small chlorospheralean (Friedmannia sp., 1.50 /tm3, Figure 6d) was abundant at the DCM, but its contribution to the biomass maximum was minor due to its
small size. Other less abundant species showed similar broadly peaked distributions
with maxima in one of the three depth ranges described above (mixed layer, mid-depths
and DCM; Lopez, 1977). The size of species showed no depth trend, with equal numbers
of large and small species occurring in deep and shallow water. However, larger and
more colonial diatom species (e.g. C. ocellata, Stephanodiscus alpinus, Fragilaria
crotonensis, Melosira italica) generally were deeper than smaller diatom species (e.g.
C. stelligera and Synedra radians).
Summer DCM dynamics
Discussion
Some DCM represent an accumulation of phytoplankton populations (population
response) and others represent an elevated cellular concentration of chlorophyll
(physiological response). Of those DCM caused by an accumulation of phytoplankton,
Cullen (1982) distinguished among accumulations caused by three effects: in situ cell
growth, sinking from overlying waters, and behavioral responses of motile species.
In addition, zooplankton may contribute to the DCM by selectively grazing
phytoplankton above the DCM layer (Venrick et al., 1973; Longhurst, 1976), although
Cullen (1982) argued that DCM can be explained without considering zooplankton
grazing.
Clearly, the DCM in Lake Tahoe was an accumulation of phytoplankton populations
near and above the compensation depth and the nitracline. Because the predominant
species in the DCM were non-motile, the behavioral mechanism of accumulation can
be disregarded. Though additional measurements are needed to distinguish between
336
From mid-July through September, the depth of the biomass maximum fluctuated between 110 and 90 m. The biomass peak shoaled twice (from 30 July to 6 August and
23 August to 10 September) and deepened twice (from 17 August to 23 August and
24 September to 9 October) during this period. The magnitude of the biomass peak
also varied over time, decreasing from a maximum of 23.9 mg C m~ 3 (15 July) to
a minimum of 7.3 mg C m~ 3 (17 August) and then increasing to 18.9 mg C m~ 3 (10
September).
The time—depth distributions for individual species further demonstrate the dynamic
character of the DCM layer, particularly during and after the storm in early August.
Most species decreased in density in early and mid-August, and then increased in density in late August and early September (e.g. C. stelligera, C. ocellata and Friedmannia sp.). The depth of maximum density for some deep species in this group (e.g. C.
ocellata) also shoaled 10—20 m. Other species (e.g. O. lacustris) showed a gradual
decrease in abundance over this period, with a slight decline in their depth of maximum density.
Summer DCM dynamics
Physical factors, particularly sinking and internal waves cannot account for the DCM
dynamics we observed during summer months. Rapid sinking (2 m day" 1 ) could explain the accumulation of C. ocellata (the summer DCM dominant) in the DCM layer
from early to mid-July, yet the DCM was sharply defined in the 90— 110 m zone in
late June (Coon, 1978). Sinking out of the DCM might have caused the decrease in
C. ocellata abundance during early August, although this would have required exceptionally high sinking rates ( > 4 m day" 1 ). The highest estimate for in situ sinking rates
of the predominant phytoplankters in Lake Tahoe is 0.5 m day" 1 (Tilzer et al., 1977).
Vincent (1977) and Lopez (1977) report even slower velocities in vitro.
337
the importance of sinking, zooplankton grazing and in situ cell growth, the evidence
presented here suggests that all three processes may contribute to the maintenance of
the DCM and that the role of in situ production is substantial.
We tested for a shade-adaptive response by phytoplankton in die DCM by comparing the C:Chl ratios of DCM and epilimnetic phytoplankton samples, and found that
the ratios were not different. Typically, a positive correlation between C:Chl and light
intensity is interpreted as a shade-adaptive response, except under conditions of extreme nutrient limitation (Bannister and Laws, 1980; Cullen, 1982). However, Falkowski
and Owens (1980) found that at least one diatom species adapts to low light intensities
not only by increasing cellular chlorophyll content, but also by decreasing cellular carbon content. If DCM species in Lake Tahoe adapt to low light intensities in this way,
they would not exhibit the predicted decline in C:Chl ratio widi the decline in light
intensity. Regardless of the physiological response of DCM phytoplankton, it is clear
that the DCM represents an accumulation of phytoplankton, and not an increase in
cellular chlorophyll content.
The vertical pattern of chlorophyll in Lake Tahoe is distinct from vertical patterns
described from other lakes (e.g. Fee, 1976). Even in large lakes such as Lakes Superior
and Michigan, the DCM forms in or directly below the thermocline and the depth of
maximum primary productivity (Brooks and Torke, 1977; Moll and Stoermer, 1982;
Fahnenstiel and Glime, 1983; Moll et al., 1984). The occasional thermocline submaximum at Lake Tahoe (e.g. 15 July and 17 September, Figure 1) may be analogous to
these maxima in odier lakes. Thermocline maxima probably result from conditions of
rapid nutrient turnover in ihe relatively stable water below the thermocline, favoring
locally high rates of primary production (Moll et al., 1984).
The summer chlorophyll structure in Lake Tahoe is more similar to structures found
in ocean systems, particularly those in the 'variable environment' classification of Cullen
(1982). These systems exhibit a DCM situated well below the deptii of maximum primary
productivity and coincident with the nitracline, as in Tahoe. However, the process by
which the Tahoe DCM was maintained through the summer differs from the process
suggested by Cullen (1982). Cullen stated that 'variable environment' DCM are relicts
of spring phytoplankton growth which have settled to a density and/or nutrient discontinuity. Abbott et al. (1984) demonstrated that the phytoplankton species composition of the Tahoe DCM in summer, 1980 was dominated by five species that were never
present in the spring productivity maximum. Moreover, the biomass profiles presented
here support die hypothesis mat the summer DCM is a dynamic layer of active cells.
T.G.Coon et at.
338
If internal waves had caused the biomass and C. ocellata maxima to shoal 20 m from
August to September, the densities in the maxima would not have decreased during
August. Furthermore, if physical factors were solely responsible for the observed
dynamics, other species would be expected to respond as C. ocellata did, yet they did
not. Friedmannia sp. did decrease in density from July to August and increased from
August to September, yet the depth of maximum density was the same from early August
through October. The second most important species (by biomass) in the biomass maximum, a 463-/im3 green alga (species undetermined), decreased in abundance from August
to September, but without a change in depth distribution (Lopez, 1977). The depth
distribution of the dominant species above the DCM, O. lacustris changed very little
from August to September. Finally, internal waves below the thermocline have
amplitudes of 1-2 m, not 1 0 - 2 0 m (Caldwell et al., 1978; Brubaker, 1979).
Other physical factors corresponded with changes in the summer depth distribution
of phytoplankton: mixing and light availability. Conditions during the months of July
and September were relatively calm, as illustrated by the temperature profiles (Figure
2). The storms in early August eroded the thermocline, most evident in the 17 August
and 23 August temperature profiles. The deeper distribution of the mixed layer dominant, C. stelligera, in mid-August and the broader distribution of O. lacustris may have
been induced by this mixing activity.
The amount of surface iiTadiance decreased and was less consistent during the stormy period. Given the limited light conditions in the DCM layer ( < 1 % / 0 ), it is possible that a decrease in light availability such as occurred in August would reduce growth
rates and/or increase respiration and death rates in the DCM layer sufficiently to cause
the observed decline in chlorophyll and biomass concentrations during August.
Zooplankton probably had little impact on the phytoplankton distribution, particularly
in August and September. Richerson et al. (1978) showed that zooplankton biomass
was three times greater in the upper 75 m of the water column than in the DCM layer.
This is consistent with the hypothesis that zooplankton grazing reduced phytoplankton
densities above the DCM; however in Lake Tahoe the zooplankton densities were so
low that they could only have a minor impact on phytoplankton abundance. Furthermore, the dominant zooplankton species, Diaptomus tyrelli and Epischura nevadensis
reached their peak abundances in late May and June in 1976 (Goldman, 1981). During
August and September, their densities were greatly reduced and were relatively constant.
The resurgence and shoaling of the DCM in September strongly supports the
hypothesis that the DCM is maintained by in situ cell growth. Neither sinking nor internal waves nor zooplankton grazing can explain these changes in the DCM. Whether
the mechanism of cell increase is due to increased growth rates or decreased loss rates
cannot be distinguished. It is noteworthy that the September increase coincided with
an increase in surface irradiance and in DCM layer nitrate concentrations (Figures 5
and 2), further supporting the hypothesis that phytoplankton cellular processes (growth
and/or respiration) were responsible for the changes in the phytoplankton populations.
The results of this study support the Vincent (1977) and Abbott et al. (1984) model
(after Dugdale, 1967) of Lake Tahoe as a two-layered euphotic zone system in the summer period. In the upper layer, phytoplankton are primarily nutrient limited. This layer
extends from the surface to the nitracline (at 75 — 110 m). The lower layer, extending
3 0 - 5 0 m deeper, is primarily light limited. The deep chlorophyll maximum defines
the transition from nutrient limitation to light limitation. Here phytoplankton are deficient in both nutrients and light, but under particular conditions, both factors may
be sufficiently available to stimulate growth and prolonged cell maintenance, resulting
in an increase in biomass and chlorophyll. Venrick (1982) showed that the phytoplankton
assemblages of these two layers are distinct in the North Pacific Central Environment,
and that the region of the DCM marks the transition between assemblages-. The results
of Lopez (1977), Vincent (1977) and Figure 6 demonstrate that a complex, vertically
structured phytoplankton assemblage also exists in Lake Tahoe. Moreover, the Tahoe
phytoplankton distributions in the two euphotic zone layers are more finely divided
by different species. The two most abundant species of the nutrient limited layer, C.
stelligera and O. lacustris exhibit differentiated depth distributions. Similarly, C. occllata
and Friedmannia sp. were slightly offset in the timing of their respective abundance
maxima.
li^t^LN
(1)
where ii^a is a constant whose value does not affect our considerations. A variety
of forms have been used for the functions L and N (Dugdale et al., 1981; Rhee and
Gotham, 1981). All have the property that they increase linearly at low light intensities
and nutrient concentrations, and saturate to a constant value at high light intensities
and nutrient concentrations (we neglected the shallow zone of photoinhibition because
we were concerned with processes occurring at low light). Because light intensity
decreases with depth, and nutrient concentrations increase with depth, expression (1)
predicts that the in situ growth rates will have a relative maximum at the depth where
l/L(dI7dz) = -l/N (dN/dz). We chose explicit forms for the functions L[I(z)] and
MS(z)L where I(z) is light intensity and S(z) is dissolved nitrate-nitrogen concentration
at depth z, and used the observed data for I(z) and S(z) (Figure 2) to evaluate this prediction. The light profile was normalized to surface light intensity, using a two-day average
over the sampling date and the preceding day. For simplicity, we chose Monod
(Michaelis-Menten) forms for both UJ) and N(S):
W(z)] = U(z)] 1 [/k + /(z)]
(2a)
N[S(z)] = [S(z)) I [K% + S(z)]
(2b)
where 4 and Ks are constants to be fitted, assuming that the DCM is at the growth
339
Phytoplankton growth in the DCM
If in situ growth is the major process involved in maintaining the summer DCM, we
expect that cell growth rates will be reduced above the DCM by nutrient (nitrate) limitation and below the DCM by light limitation, resulting in a relative growth rate maximum at the DCM. Thus we hypothesize that the DCM depth coincides with the depth
where phytoplankton growth rates peak. To evaluate this hypothesis, we used a simple
estimate of in situ phytoplankton growth in Lake Tahoe to determine if the estimate
can accurately predict the position of the DCM, and if the physiological parameters
used in the prediction are empirically reasonable (we made no attempt to describe the
shape of the chlorophyll versus depth curve).
We assumed that the growth rate, /i, can be described as the product of two terms:
one incorporating the effects of light intensity, L (e.g. Jassby and Platt, 1976); the other
incorporating the effects of dissolved nutrient concentrations, N (e.g. Dugdale, 1977):
T.G.Coon el al.
340
rate maximum. Jassby and Platt (1976) recommended an hyperbolic tangent form for
L(7), but curves of the Monod form are sufficiently similar to the shape of the hyperbolic tangent that general conclusions are unaffected by using the simpler form. Specific
predictions of the position of the maximum may change slightly if the more accurate
Jassby-Platt form were used.
A number of previous studies have established values for Ks, the half saturation constant for nitrate uptake, and 1%, the half saturation constant for carbon uptake per unit
chlorophyll in several environments. Analogous measurements for ATS and 4 that
describe cell growth directly in terms of nitrate concentration and light intensity are
much less common. Falkowski et al. (1985) obtained an approximate range for 4 (cell
growth in units of/iEin m~ 2 s" 1 ) of 100 < 4 ^ 150 in laboratory experiments with
a diatom, a chrysophyte and a dinoflagellate species. At steady state, the kinetic
parameters for nutrient uptake and cell growth must be identical (Goldman and Glibert,
1983). For much of the period of this investigation, after the DCM had formed, and
during the period when it was being maintained, phytoplankton populations were probably close to steady state. Accordingly, the approximate range (Valiela, 1984, p.52)
of 0.1 <,KS (in /tM) s 1.0 for nitrate uptake in oceanic waters provides an adequate
initial estimate of Ks.
Any choice of values for Ks and 4 that allow the two parameters to remain within
the data-based limits (100 :£/ k < 150, 0.5 ^Ks s 1.0) predicted a growth rate maximum between the depths of 80 and 120 m. However, the values for 4 and Kt that best
predicted the location of the DCM observed in this study were 40 /iEin m~ 2 s" 1 and
0.05 /iM respectively. These were obtained by a simple grid-search least-squares procedure to find the 'optimum' 4 and Ks values, i.e. those values which minimized the
distance between the predicted and observed positions of the DCM. Predicted positions (Figure 1) were closest to observed positions in summer months. The root mean
square deviation of the predicted DCM depth from the observed maximum was 5 m
for 10 profiles. Only nine profiles shown in Figure 1 were included because two were
accompanied by incomplete chlorophyll (1 July 1976) or light (17 September 1976)
profiles, two (22 November 1976 and 27 January 1977) showed no chlorophyll peaks,
and one (21 April 1977) had a predicted peak that was significantly below the measured
maximum (at 60 m). A 10th profile, from 7 July 1976, was added to this analysis,
but was not included in Figure 1 because phytoplankton samples were not collected
with the chlorophyll profile. The only day when the predictions of equations (1) and
(2) erred by more than 10 m, 21 April 1977, was in the period when the DCM was
forming and a completely different set of processes, notably vertical mixing, dominate
the system (Abbott et al., 1984).
Our estimate of 4 (for growth) was lower by a factor of 2 —4 than that found by
Falkowski et al. (1985). Given the approximate nature of these calculations and given
that 4 values differ between species and that the laboratory experiments of Falkowski
et al. did not extend to the low light levels encountered in the DCM region of Lake
Tahoe, 4 = 40 /tEin m~ 2 s" 1 may be a reasonable estimate for cell growth in the
Tahoe DCM region. Moreover, batch and semi-continuous culture studies at low light
intensity (Chan, 1978) indicate that 4 (for growth) in several diatom and dinoflagellate
species decreases as ambient light decreases. In addition, the value of 4 = 40 /tEin
m~ 2 s~ ! is close to the lower limit of the range that Harris (1978) gives for photo-
Conclusions
Our evidence leads us to the conclusion that die summer DCM is maintained primarily
by in situ growth and secondarily by sinking of cells from water immediately above
the DCM. We suggest that the slow carbon uptake rates in the DCM, combined with
reduced loss rates (respiration, death, grazing) in diis dark, nutrient-enriched layer allow
for more efficient conversion of photosynthate into new cells (Fee, 1976; Goldman
etal., 1979; Tilzer, 1984; Forsberg, 1985). Reduced sinking rates in this region probably contribute to the accumulation of phytoplankton (Steele and Yentsch, 1960; Smayda,
1970).
The diversity of phytoplankton species found in the DCM layer may indicate that
different species capitalize on the special conditions in this environment in different
ways. Vincent and Goldman (1980) have shown that certain deep populations of Friedmannia sp. and another green ultraplanktonic species, Monoraphidium contortum
(18.2 /im3) are capable of substantial heterotrophic production. The magnitude of this
form of production at in situ concentrations of dissolved organic matter has not been
determined, but even low levels would contribute to the phytoplankton biomass.
The community-level C:Chl ratio used to test for shade adaptation is too coarse to
detect differences between species. In particular, C. ocellata dominates DCM biomass
estimates to die extent that if smaller or less abundant species such as Friedmannia
sp. or the 463-/tm3 unknown green alga had increased cellular chlorophyll content, it
would not be detected.
Sinking rates are positive functions of phytoplankton cell and colony size (Porter,
1977), but they also can be manipulated by flagellates, diatoms, blue-greens and greens
by a variety of mechanisms in response to light and/or nutrient gradients (e.g. Steele
and Yentsch, 1960; Tilzer, 1973; Smayda, 1974; Walsby and Klemer, 1974; Titman
and Kilham, 1976; Burns and Rosa, 1980). The predominance of larger diatom species
and colonies (e.g. C. ocellata) in the DCM layer and of smaller diatom species (e.g.
C. stelligera) in the mixed layer (Lopez, 1977), suggests that size-dependent sinking
rates may be important for diatom species in the DCM. Yet sinking has virtually no
influence on die small green ultraplanktonic species. Some small green species, e.g.
341
synthetic carbon uptake, 60 < / k (jiEin m~2 s~ l ) < 150. Finally, our values of / k (as
well as in situ light intensity at the DCM) are greater than the low range of values
of the compensation photon flux density (PFD) for growth, i.e. the light intensity at
which 11 = 0. For example, Falkowski and Owens (1980) and Geider et al. (1986)
found compensation PFD of 0.32 fiEin m~ 2 s" 1 and 0.5 /xEin m~ 2 s~l, respectively,
for two diatom species.
The value of Ks (0.05 /iM) is lower than that found for the half saturation constant
for nitrate uptake in the oligotrophic tropical Pacific (0.1—0.2 /tM; Valiela, 1984).
However, when growth and uptake are not in balance, Ks (growth) is thought to be
less than that for uptake (Kilham et al., 1977); this may account for our low value of Ks.
The dominance of in situ growth in maintaining the DCM is a plausible hypothesis,
but a minor role for local sinking effects cannot be ruled out. Indeed, the low 'optimum' value of 4 may indicate that the growth rate maximum may be a few meters
above the DCM, and the deeper location of the DCM is a result of sinking from this
region.
T.G.Coon et at.
Interfilumparadoxum (4.2 /tm3), were concentrated in the mixed layer. More detailed
analyses of the dynamics of individual populations in the DCM are needed to determine the importance of these different mechanisms on the dynamics of DCM
phytoplankton.
Acknowledgements
We thank M.Abbott, R.Richards, M.Otto, E.de Amezaga, W.Harrison, P.McAuliffe,
P.Neale, T.Platt, W.Vincent, C.Lovejoy, M.Tilzer and J.Jones for help in the field
or comments on this work. Two anonymous reviewers made valuable suggestions on
the manuscript. P.Hunter and the Division of Environmental Studies Computation Facility staff aided in data analysis. Financial support was provided by the National Science
Foundation, NSF-DEB75-14273, NSF-DEB76-20341 and NSF-AEN74-22675 A01 and
by the National Aeronautics and Space Administration, NAG5-217.
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