Notes
Limnol. Oceatzogr., 38(8). 1993, 1813-1818
(0 1993, by the Ameruzan Society of Limnology
and Oceanography.
1813
Inc
Chlorophyll a concentrations in the North Pacific: Does a
latitudinal gradient exist?
Abstract -Chlorophyll
a concentrations
were
measured as a function of depth from 28 to 48”N
along 152”W in March 199 1 with Whatman GF/F
and 0.2~pm Nuclepore filters. Surface Chl a concentrations measured with 0.2~ym Nuclepore filters were
up to fourfold higher than those measured with
Whatman GF/F filters. The largest difference between the two filter types was found in subtropical
waters, where picoplankton were a major constituent
of the phytoplankton
assemblage. Chl a concentrations integrated from 0 to 175 m showed a threefold
increase (9-26 mg Chl a m-I) between 28 and 48”N
when Whatman GF/F filters were used. However,
integrated Chl a concentrations based on measurements with 0.2~pm Nuclepore filters were nearly constant (25-3 1 mg Chl a mpZ) over the transect. These
results lead us to question the existence of previously
reported latitudinal
gradients in integrated Chl a
concentrations in the North Pacific Ocean.
Attempts to understand the ocean’s role in
global climate change require accurate estimates of phytoplankton
biomass and production. Recent work has shown that picoplankton constitute
a major fraction
of the
phytoplankton
biomass in tropical, subtropical, and temperate waters. As well, these small
phytoplankters have been found to contribute
significantly to the primary production in openocean ecosystems (Li et al. 1983; Platt et al.
1983). However, in oligotrophic tropical and
subtropical waters, where picoplankton dominate, Chl a concentrations and the level of
primary production may have been underestimated due to the use of filters with inappropriate pore sizes.
Numerous comparative studies of the reten-
Acknowledgments
We thank the captain, officers, and crew of the NOAA
ship Discoverer for their cooperation and assistance during
the cruise. We are grateful to Larry Small, Barry and Ev
Sherr, and two anonymous reviewers for their helpful suggestions and comments.
This research was supported by a NASA graduate student fellowship in global change research to M.-L.D. and
a NOAA climate and global change grant (NA 16RC00901) to P.A.W.
tion properties of glass-fiber and membrane
filters have demonstrated that glass-fiber filters
inadequately retain < 1-pm-diameter cells due
to their large nominal pore size (0.7 and 1.2
pm for Whatman GF/F and GF/C filters). Low
retention efficiencies of glass-fiber filters result
when Chl a concentrations are low (<0.5-l .O
pg Chl a liter-‘) and when picoplankton are a
dominant fraction of the phytoplankton
assemblage (Phinney and Yentsch 1985; Taguchi
and Laws 1988). Under such conditions the
use of membrane filters with submicron pore
sizes has been recommended (although not always followed). Many studies have made extensive use of glass-fiber filters due to their low
cost and fast flow rates.
Results from previous basinwide studies
have suggested the presence of a latitudinal
gradient in integrated Chl a concentrations between subtropical and subarctic waters. The
purpose of this study was to compare Chl a
concentrations in subtropical, transition, and
subarctic waters and to evaluate the existence
of a meridional gradient in integrated Chl a
concentrations across the North Pacific basin.
Sampling was conducted from 20 to 55”N
along 152”W in March 199 1 on the RV Discoverer as part of the Climate and Global
Change Program of NOAA. Water samples
were collected at -20-m intervals from the
surface to 100 m and then every 25 m to a
depth of 175 m with lo-liter Niskin bottles
attached to a rosette sampler. Duplicate 200ml subsamples of seawater were filtered under
low vacuum pressure (5 180 mm of Hg) onto
either 25-mm-diameter
combusted Whatman
GF/F or 0.2~pm Nuclepore filters. Near the
end of the filtration, 0.5 ml of saturated MgC03
was added to the samples. Chl a concentrations were measured with a Turner Designs 10
fluorometer after a 24-h extraction in 90% acetone at -20°C in the dark. Before the cruise,
the fluorometer was calibrated with a pure Chl
a standard purchased from Sigma Chemical
Co. In addition, the fluorometer was also stan-
1814
Notes
dardized before each use with a secondary Chl
a standard, also from Sigma Chemical Co., and
with 90% acetone blanks and extracted filter
blanks (Whatman GF/F and Nuclepore filters)
(Venrick 1987). Integrated Chl a concentrations were calculated with the trapezoid method of integration. The vertical profile of the
Chl a concentration at 32”N, 152”W was not
included in Fig. 1 because some of the samples
may have been mixed. However, there was
no significant effect on the integrated Chl a
concentrations.
The mean precision * 1 SD
for duplicate
Chl a measurements
was
0.025+0.017 for GF/Ffiltersand
0.015*0.004
for 0.2~pm Nuclepore filters.
In September 199 1 during a cruise off northern California, we used the same procedure
outlined above to test if a difference could be
detected in the amount of Chl a measured by
combusted
and noncombusted
Whatman
GF/F filters. We also checked whether lower
vacuum pressure (80 mm of Hg) increased the
amount of Chl a measured. The station selected for these tests was 650 km off northern
California (42”N, 132”W) in oligotrophic waters characterized by low ambient nitrate concentrations (- 1 ,uM) and a low phytoplankton
standing stock (-0.080-0.300
pg Chl a liter- l). This site was chosen for its similarity
to stations in subtropical waters along the
NOAA transect.
Comparison of combusted with noncombusted Whatman GF/F filters showed no appreciable difference in the Chl a concentrations
measured for two depths at the oligotrophic
site off northern California (Table 1). Chl a
concentrations were found to be -7% lower
when the vacuum pressure was 80 mm of Hg
compared to 180 mm of Hg. Chl a concentrations measured at 15 and 100 m were comparable to those encountered at the southern
end of the NOAA transect. The results of these
tests indicate that the low Chl a values for the
Whatman GF/F filters during the NOAA transect were not due to increased porosity of the
combusted Whatman GF/F filters, inappropriate vacuum pressures, or a combination of
the two.
Vertical profiles of Chl a concentrations at
four stations extending from the central North
Pacific gyre (28”N), through the transition zone
(37”N), and into subarctic waters (42 and 48”N)
showed very different patterns (Fig. 1). Surface
Chl a concentrations measured with Whatman
Table 1. Comparison of Chl a retained by combusted
and noncombusted Whatman GF/F filters and by combusted filters at vacuum pressures of 80 and 180 mm of
Hg. Duplicate samples were compared for each treatment.
The overall precision (SD) for these measurements was
0.01, n = 6.
GF/F filters
(noncombusted/
combusted)
Depth
Cm)
15
100
Mean + SD
Combusted
filters
(80/ 180 mm of Hg)
0.97
1.10
1.04+0.09
0.92
0.93
0.93*0.01
GF/F filters were lowest in the subtropical waand highest in
ters (0.023 pg Chl a liter’)
subarctic waters (0.299 pg Chl a liter-l).
A
deep, subsurface Chl a maximum layer (0.2500.300 pg Chl a liter-l) was located between
100 and 120 m in the subtropical and transition waters but was absent in the subarctic
water at 48”N. The 0.2~pm Nuclepore filters
retained 3-4 times more Chl a than the Whatman GF/F filters in subtropical waters and 23 times more Chl a in the transition zone. Chl
a concentrations measured with 0.2-pm Nuclepore filters were not different from those
measured with Whatman GF/F filters below
100 m in the subarctic (48”N). However, in the
upper 100 m the difference in the Chl a concentrations between the two filter types was
significantly
different from zero (Student’s
t-test, P < 0.001). The relative picoplankton
abundance in the Chl a maximum layer was
highest in subtropical water (85% of the total
Chl a), intermediate in transition water (78%
of the total Chl a), and lowest in subarctic
water (35-48% of the total Chl a) (Table 2).
Chl a concentrations integrated from 0 to
175 m (Fig. 2) showed a threefold increase (926 mg Chl a m-*) between 28 and 48”N when
Table 2. Percent abundance of picoplankton Chl a in
the Chl a maximum layer of subtropical, transition, and
subarctic waters. The percentage of Chl a in the 0.2-3-pm
fraction was calculated by [( >0.2 pm - > 3 pm)/>0.2 pm]
x 100%. ND-No
data.
>0.2 I.trn
>3 I.rrn
% Chl a
(0.2-3-wrn
fraction)
0.244
0.211
0.293
0.350
0.382
0.037
0.047
ND
0.228
0.200
84.8
77.7
ND
34.9
47.6
Chl a (kg liter
N lat
28”
32”
37”
42”
48”
Depth
(m)
100
20
100
40
6
‘)
Notes
1815
Chl a (1.19liter-‘)
Chl a (pg liter-‘)
0
0.10
I
I
0.20
I
I
0.30
i
40 -
160
ISO/-\
Chl a (pg liter-‘)
0.10
/
o-o
GF-F
o--o
Nuclepore
Chl a (pg liter-‘)
0.20
, -
120
I
I
I
160
;I’
I
Fig. 1.
Nuclepore
Vertical
filters.
42”N
152” W
o-o
GF-F
@
Nuclepore
profiles of the Chl a concentrations
at four locations
obtained with Whatman
GF/F and 0.2-hrn
1816
Notes
Whatman GF/F filters were used. However,
integrated Chl a concentrations
for phytoplankton retained on the 0.2-pm Nuclepore
filters were relatively constant along the transect (25-31 mg Chl a m-2). This result was
due to a significant fraction of the Chl a in
subtropical
and transition
waters passing
through the Whatman GF/F filters but being
retained by the 0.2-pm Nuclepore filters.
Many investigators have been concerned
about the loss of cells through glass-fiber filters
and the magnitude of the problem. Most comparative studies have concluded that membrane filters retain more Chl a than glass-fiber
filters, especially when Chl a concentrations
are ~0.5-1 .O pg Chl a liter-l (Venrick and
Hayward 1984; Phinney and Yentsch 1985).
Munawar et al. (1982) found that 42% more
Chl a was retained by 0.2-pm Nuclepore filters
than Whatman GFK filters. Similarly, Venrick et al. (1987) reported that 0.45-pm Millipore HA filters measured 27% more Chl a
than Whatman GF/C filters at 24”N in the Pacific. At 47”N the difference between the filter
types was 10%. Phinney and Yentsch (1985)
compared Chl a retention by 0.45~pm Millipore HA membrane filters with various types
of glass-fiber filters in laboratory and field experiments. In their studies with cultured phytoplankton from four oceanic regions, they
found no significant difference in the Chl a
concentration measured with either the 0.45pm Millipore HA or Whatman GF/F filters.
However, Whatman GF/F filters were found
to be inadequate and gave variable results when
used in a series of field experiments where Chl
a concentrations were in the range of O-5 pg
Chl a liter- l. Phinney and Yentsch concluded
that under low biomass conditions the most
efficient glass-fiber filters retained only 60% of
the Chl a.
Our data confirm that membrane filters have
superior retentive properties compared to glassfiber filters but also indicate that the magnitude
of the difference between the two filter types
in subtropical waters may be greater than previously thought. The 0.2-pm Nuclepore filters
retained 67 and 74% more Chl a than the
Whatman GF/F filters at 28”N in the chlorophyll maximum layer and in the surface water,
respectively.
However, this difference was
smaller at higher latitudes. At 48”N there was
only a 1O-27% difference between the two filter
types.
I
30c-7
‘E
-s”
5
T<
//
20-
n
w
5
g
it
/
_
P
//
-
/
\
/
‘\
/
‘0’
/
io-
GF-F
/
d
t
t
01
I
20
I
30
I
LATITUDE
I
40
I
50
(“N)
Fig. 2. Integrated Chl a concentrations (mg Chl a m ?)
from 0 to 175 m between 28 and 48”N, 152”W calculated
from Chl a concentrations determined with Whatman GF/F
and 0.2~pm Nuclepore filters.
Past work has indicated the existence of a
steep latitudinal
gradient in phytoplankton
species composition, biomass (McGowan and
Williams 1973) and in situ fluorescence of Chl
a (Pak et al. 1988) extending from the central
North Pacific subtropical gyre to subarctic waters. Originally, this gradient was defined on
the basis of differences in the surface Chl a
concentration between subtropical and subarctic waters. In our study, surface Chl a concentrations also showed a latitudinal gradient
between southern and northern ends of the
transect, regardless of the type of filter used.
Data suggesting the presence of a latitudinal
gradient in integrated Chl a concentrations were
based on a series of basinwide cruises along
155”W that took place from 1960 to 1980.
Results from these cruises have been reported
elsewhere (Hayward and Venrick 1982; Hayward et al. 1983; Hayward and McGowan
1985; Hayward 1987). During these cruises
were measured with
Chl a concentrations
Whatman GF/C filters. The latitudinal pattern
that emerged from these data sets agrees with
our integrated values obtained with Whatman
GF/F filters. However, our integrated >0.2pm Chl a data indicate that a latitudinal gradient between subtropical and subarctic waters
is weak at best when the picoplankton component of the phytoplankton assemblage is included. Pak et al. (1988) reported meridional
variations in Chl a concentrations along 15 5”W
in the North Pacific. Their fluorometric data
show an increase in relative fluorescence between 23” and 57”N, however their extracted
pigment results indicate no difference between
Notes
vertically integrated pigment concentrations at
28” and 42”N. It is not clear at present whether
in situ fluorescence can be used as a proxy for
extracted Chl a.
Unfortunately
there are no other basinwide
data sets that include submicron Chl a with
which we can compare our results with Nuclepore filters. Nonetheless, the integrated Chl
a concentration measured over O-200 m at one
station (28”N, 155”W) with 0.45~pm Millipore
HA filters during the PRPOOS experiment was
-26 mg Chl a m-2 (Venrick et al. 1987). This
value closely corresponds to our estimate of
25 mg Chl a rnA2 at 28”N, 152”W from 0 to
175 m obtained with 0.2-pm Nuclepore filters,
and both values exceeded the Chl a trapped
on Whatman GF/F filters by almost a factor
of three.
We can only presume that the component
of the picoplankton assemblage retained by the
0.2~pm Nuclepore and not the Whatman GF/F
filters consisted of a marine prochlorophyte,
Prochlorococcus. The largest discrepancy in the
Chl a concentrations between filter types was
found at the lower latitudes along the transect,
in nutrient-poor water. This pattern is consistent with other studies reporting this taxonomic group to be numerically abundant in oligotrophic waters (Olson et al. 1990) and to
contain a large fraction of the Chl a below the
mixed layer (Campbell et al. unpubl.). As well,
the small size of prochlorophyte
cells (Chisholm et al. 1988 report a mean cell diam of
0.7 pm) makes it likely that a significant portion of the prochlorophyte
population passed
through the glass-fiber filters. If prochlorophytes were primarily responsible for the observed differences in Chl a concentrations, it
raises the possibility that the difference between filter types might actually be larger than
that observed, due to the presence of Chl b
(Chisholm et al. 1988). Significant quantities
of Chl b can cause overestimation in pheopigment concentrations and result in underestimation of the Chl a concentration (Loftus and
Carpenter 197 1). However, LeBouteiller et al.
(1992) found no bias in the Chl a estimation
arising from the presence of Chl b as long as
the ratio of Chl b : Chl a is < 1. They further
report a maximum Chl b concentration in deep
subtropical water where the Chl b : Chl a is
-0.2. Thus, it seems unlikely that our Nuclepore results were influenced by the presence
of Chl b.
1817
Our results suggest that historical data sets
may have underestimated
Chl a concentrations in subtropical and transition waters by a
factor of two to four whenever glass-fiber filters
were used. Primary production measurements
also may have been underestimated due to the
loss of small cells through glass-fiber filters.
The magnitude of the underestimation may be
significant when one considers that there is a
linear relationship between integrated Chl a
concentrations
and integrated primary production (Hayward and Venrick 1982) and
-60% of the primary production in tropical
and subtropical waters can be attributed to picoplankton (Li et al. 1983; Platt et al. 1983;
Iturriaga and Mitchell 1986). Obviously, there
is a serious need to use filters with submicron
pore sizes in low biomass waters to ensure accurate measurements of phytoplankton standing stocks and primary production.
Mary-Lynn Dickson’
Patricia A. Wheeler
College of Oceanic and Atmospheric
Oregon State University
Corvallis 9733 l-5503
Sciences
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I Present address: Graduate School of Oceanography,
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1818
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Inc
Planktivore effects on zooplankton epibiont communities:
Epibiont pigmentation effects
Abstract-We
observed the development of epibiont communities on freshwater crustacean zooplankton from 12 July-3 1 August 1991 in three
ponds: one with planktivorous
fish, a second with
planktivorous
larval salamanders, and a third with
planktivorous
fish added midway through the sampling period. Prevalence, on zooplankton,
of pigmented euglenoid epibionts (Colucium vesiculosum),
alone and with unpigmented peritrich ciliates (Vorticella campanula and Epistylis sp.), was significantly
reduced by the addition of planktivorous
fish in the
third pond, while the prevalence of peritrich ciliates
alone was not. Neither of the ponds with unaltered
planktivore
regimes showed a similar pattern of
change in prevalence of pigmented and unpigmented
epibionts on zooplankton. The relative loss of pigmented euglenoid epibionts, after planktivore
addition, suggests that epibiont color or contrast may
increase the susceptibility of their substrate organisms to planktivores.
Acknowledgments
We thank Phil Mason and Terry Schneider for assistance, and D. A. Chiavelli for editorial comments.
This study was funded, in part, by a grant from the
Colorado Division of Wildlife for monitoring salamander
populations in western Colorado.
Epibionts on zooplankton are thought to increase the visibility and vulnerability
of their
substrate organisms to visually
orienting
planktivores (Green 1974; Evans et al. 1979;
Willey et al. 1990; Chiavelli et al. 1993). The
effect of epibionts on zooplankton visibility
seems obvious (Fig. l), has been long suggested
(Green 1953, 1974), and is supported by related work which shows that eyespots and other forms of cladoceran pigmentation affect susceptibility to predators (Zaret 1972; Mellors
1975; Konecny et al. 1982). Experimental work
demonstrating that epibiont-enhanced
visibility is a mechanism of increased vulnerability
to planktivores is still lacking (Threlkeld et al.
1993).
In a series of subalpine ponds in Colorado,
we observed that many epibiotic taxa, including some pigmented photosynthetic
(e.g. Colacium vesiculosum) and some unpigmented
heterotrophic taxa (e.g. Vorticella campanula),
often coexist on the same substrate organisms
(Threlkeld
and Willey
1993; Willey and
Threlkeld 1993). Here we present evidence that