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Abundance and distribution of
nanoplankton in the epipelagic
subtropical/tropical open Atlantic Ocean
G.-A. PAFFENHÖFER*, M. TZENG, R. HRISTOV, C. L. SMITH AND M. G. MAZZOCCHI1
SKIDAWAY INSTITUTE OF OCEANOGRAPHY, SAVANNAH, GA
31411, USA AND 1STAZIONE ZOOLOGICA ‘ANTON DOHRN’, VILLA COMUNALE,
80121 NAPOLI, ITALY
*CORRESPONDING AUTHOR:
[email protected]
The objective of this research was to quantify the abundance and distribution of nanoplanktonic
particles available to frequently occurring juvenile and adult planktonic copepods in the epipelagial
of the open subtropical and tropical ocean. We chose locations off Puerto Rico and off the Bahamas
to achieve our purpose. The hydrography for all stations revealed a thin upper mixed layer, a
thermocline with varying temperature decreases, salinities approaching and surpassing 37%, and
chlorophyll concentrations increasing with depth from 0.05 to 0.25 g l 1. Nanoplankton was
grouped into five size ranges from 2–4 to 10–20 m equivalent spherical diameter (ESD), and
four cell types (photosynthetic nanoflagellate, Pnano; heterotrophic nanoflagellate, Hnano; photosynthetic dinoflagellate, Pdino; heterotrophic dinoflagellate, Hdino). The 10–20 m range had the
highest total cell volume, and the 8–10 m range the lowest values; for cell type, volumes of Pnano
and Hdino were highest, and Hnano lowest. Total particle concentrations covering all depths and
stations ranged from 3.4 to 17.5 g C 11. At a large percentage of sampled depths total cell
volumes of heterotrophs came close to those of autotrophs. Total autotroph volume was higher in the
smaller size ranges than in the larger ones, while the opposite was found for heterotrophs.
Calculations for ingestion rates of females of the oceanic calanoid Paracalanus aculeatus at
environmental food levels and size distributions revealed that the 10–20 m ESD particle size
fraction contributed between 46 and 82% of the total ingested nanoplanktonic cell C. At nearly all
the observed abundances in our study this copepod would obtain sufficient amounts for basal
metabolic needs, and at the majority of stations and depths have additional energy assimilated to
cover enhanced metabolic demands and limited reproduction.
INTRODUCTION
The quality and quantity of particles in the ocean and
their variability determine to a considerable extent
which zooplankton taxa (proto- and metazooplankton)
can exist and which may persist. An evaluation of particle size distribution in the open ocean according to
latitude revealed differing particle size spectra (Sheldon
et al., 1972). The spectra from cooler climates were
marked by abundance peaks of various larger particles,
while those from subtropical and equatorial regions were
rather even, i.e. more or less flat. Since these spectra by
Sheldon et al. (Sheldon et al., 1972) have a logarithmic
scale on the x-axis, a linear scale would imply a decrease
of volumetric abundance from small to large particle
sizes. This means that there would be more particle
volume per milliliter for the 2–4 mm range than the 4–
6 mm range, and more in the 4–6 mm than in the 6–8 mm
ESD (equivalent spherical diameter) range in those
warm water regions.
In those open ocean, warm water regions, small copepod genera whose adults hardly surpass 1.0 mm prosome length dominate by number [e.g. (Roman et al.,
1995; Webber and Roff, 1995a)], and appear to be
similar in biomass as compared with larger taxa [daytime biomass of 64–500 mm versus 500–2000 mm
zooplankton for the upper 200 m (Roman et al., 1995;
White et al., 1995)]. Such small copepods and their
juveniles are known to ingest particles from near 2 to
beyond 30 mm ESD [e.g. (Bartram, 1981; Paffenhöfer,
doi: 10.1093/plankt/fbg106, available online at www.plankt.oupjournals.org
Journal of Plankton Research 25(12), Ó Oxford University Press; all rights reserved
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1984; Berggreen et al., 1988)] i.e. mostly particles in the
range of nanoplankton. Nauplii and copepodid stage I of
Paracalanus quasimodo cannot ingest particles wider than
12 mm (G.-A. Paffenhöfer, personal observation). With
increasing stage, larger particles can be ingested while
small particles become less significant as food because
they are not as well perceived anymore and therefore
are not as often actively captured as [e.g. (Price and
Paffenhöfer, 1985)]. All this implies that food particles in
the nanoplankton size range are of major significance for
juveniles to adults of many of the copepod species in the
epipelagic subtropical and tropical open ocean.
The data from Sheldon et al. (Sheldon et al., 1972) and
others indicate continuously low particle abundances in
the nanoplankton range in the warm open ocean, as also
observed by Caron et al. (Caron et al., 1995, 1999) off
Bermuda, Verity et al. (Verity et al., 1996) and Calbet et al.
(Calbet et al., 2001) for the equatorial Pacific, and
Dennett et al. (Dennett et al., 1999) for the open Arabian
Sea. Since different particle sizes and types can be
ingested at different rates by different species of planktonic copepods, and again differently by their juvenile
stages, our objectives included: (i) quantifying the abundance of different size groups within the nanoplankton
range at various depths of the epipelagial; (ii) determining the cell types which made up the nanoplankton; and
(iii) using the results from the above mentioned research
to determine the contribution of environmentally available particles of different size to the diet of a subtropical/
tropical calanoid.
We chose as our study area the western part of the
northern subtropical gyre of the north Atlantic Ocean,
in particular north of Puerto Rico and east of the Bahamas
(Figure 1). These waters are part of the Antilles Current,
which partly represents the continuation of the North and
South Equatorial Current (Tolmazin, 1985).
METHOD
We conducted our sampling for nanoplankton abundance and vertical distribution in oligotrophic waters
off Puerto Rico (19 N; 66 W) on May 31 and June 2,
2001, and the Bahamas (25 N; 70 W) on June 7 and
June 9, 2001, each collected near 0700 h EST (Figure 1).
One sampling cast was conducted on each date, for a
total of four casts. For each cast, we collected water
samples with 10 l Niskin bottles deployed on a CTD
rosette. We collected water at 15, 45, 75, 105, 120 and
140 m, and quantified profiles of temperature, salinity
and chlorophyll with each cast.
To calibrate the in vivo chlorophyll data obtained with
the CTD fluorometer (SeaTech), we collected and analyzed water samples from eight additional CTD casts for
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chlorophyll a (Chl a) (Parsons et al., 1984), four each from
off Puerto Rico and the Bahamas. These water samples
originated from 0, 30, 60, 75, 90, 105 and 120 m depth.
For each depth we filtered 250 or 300 ml of water
through a 25 mm Whatman GF/F filter. Filters were
wrapped in foil and preserved by freezing at 20 C for
analysis after the cruise. We filtered two water samples
for each depth and averaged the Chl a values from
each depth. To compare in vivo data from the CTD
fluorometer with in vitro filter data, we combined the
data from all depths by calculating a linear regression:
y = 0.51x + 0.001, r2 = 0.88; y = in vitro Chl, x = CTD
fluorometer voltage reading.
To obtain a representative sample of unicellular
organisms from each depth, a subsample of 150 ml of
water was filtered through a 0.8 mm filter, after buffering
with 3.75 ml of glutaraldehyde (250 ml per 10 ml sample).
The filter was then stained with Proflavin and DAPI.
Proflavin stains cellular material and fluoresces green
under blue light of a narrow wavelength (515 nm), in
contrast to Chl which appears red. DAPI stains nuclear
material and fluoresces under ultraviolet (UV) light
(397 nm). The prepared filter was mounted on a slide
with immersion oil and preserved by freezing at 20 C.
We prepared two slides for each depth, each containing
nano- and microplankton from 150 ml of water. This
approach resembles that of Verity et al. (Verity et al.,
1996).
Slides were examined between 6 months and 1 year
after preparation, under oil immersion at 600, using
a compound microscope with a color QRetiga digital
camera connected to a computer running QImaging
software. For each slide, at least 50 sets of digital images,
representing 50 fields of view, were captured. Each set
included images viewed with Narrow Blue wavelength
band (NB) and UV light. Fifty fields of view at 600
cover 0.36% of the total filter area.
We analyzed the images using Skipper (http://mapple.
skio.peachnet.edu/skipper), an image analysis software
system for scientific research developed by R. Hristov.
Cells that ranged in size from 2 to 20 mm ESD were
counted, measured, and classified by broad taxonomic
group and trophic level. Estimations of ESD and biovolume for each cell were automatic functions of Skipper,
based on manual outlining of cell boundaries. We calculated Carbon (C) from biovolume measurements using
the methods of Caron et al. (Caron et al., 1999).
We classified cells into the following categories:
photosynthetic nanoflagellate (Pnano), heterotrophic
nanoflagellate (Hnano), photosynthetic dinoflagellate
(Pdino) and heterotrophic dinoflagellate (Hdino). Diatoms and ciliates were also noted when found, but
were not sufficiently numerous between 2 and 20 mm
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Fig. 1. Map of the Atlantic Ocean between 15 and 30 N, and 60–80 W.
ESD to be included in statistical analyses. Using the NB
images, cells were determined to be autotrophic if they
were red, and heterotrophic if they were green. In general, cells <5 mm ESD were classified as nanoflagellates,
although some diatoms can be found in that category.
For cells >5 mm ESD, we used the UV images to
determine whether the cell had a small or indiscernible
nucleus (nanoflagellate) or a large nucleus (dinoflagellate).
Most Hdinos had a characteristic elliptical shape while
most Pdinos were spherical. Diatoms were elongated
autotrophs, usually with an obvious frustule; most were
needle-shaped. Heterotrophs >8 mm ESD with obvious
cilia, or unusual shapes and arrangements of nuclei, were
classified as ciliates. We also observed a significant number of Hdinos ingesting autotrophs. Cells were subdivided
into five size range classes: 2–4, 4–6, 6–8, 8–10 and 10–20
mm ESD.
We applied Friedman’s test to analyze differences in
total particle concentration as well as cell sizes and cell
types. This test is a randomized block analysis of variance by ranks (Zar, 1974; Conover, 1980). If the null
hypothesis was rejected, we followed with a multiple
comparison analysis (Conover, 1980).
To quantify the daily ingestion rates of nanoplankton
by adult fertilized females of Paracalanus aculeatus, a small
copepod occurring abundantly in outer shelf and oceanic
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Fig. 2. Hydrographic observations at four stations in the tropical and subtropical Atlantic Ocean (temperature, salinity, chlorophyll).
Table I: Nanoplankton (2–20 m ESD) concentrations at four locations at different depths expressed
as g C l 1
Depth (m)
Casts
11a
19
35
41
15
7.2
12.8
13.5
45
7.8
12.7
10.3
3.4
75
10.3
12.3
8.8
7.1
105
6.8
9.1
17.5
5.8
120
7.9
8.8
6.3
11.2
140
7.9
9.2
–
12.1
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Fig. 3. Abundance and vertical distribution of cells from different size ranges at four stations.
waters off the south-eastern USA (Bowman, 1971), and in
oceanic waters off Jamaica (Webber and Roff, 1995a), we
conducted a series of feeding rate experiments to establish
a relationship between clearance rate and food particle
volume. This could then be applied to the five cell ranges
from our nanoplankton quantifications. We simultaneously offered phytoplankton at 4.5 (Isochrysis galbana),
8.2 (Rhodomonas sp.) and 11.8 mm (Thalassiosira weissflogii)
in diameter (ESD) at 20 C, at average concentrations of
~5 mg C l1 for 20–24 h. These conditions resemble
particle concentrations in the subtropical/tropical epipelagial, implying that the copepods were heavily food limited and at their maximum particle perception abilities;
therefore they would be feeding at the highest clearance
rates they could achieve (Paffenhöfer and Lewis, 1990),
resulting, by multiplication with the average food concentrations, in ingestion rates under oligotrophic conditions.
The particle concentrations at the beginning and end of
the experiments were quantified by inverted microscope
counts or with a Coulter Counter. We usually had two
experimental and one control jars, each of 960 ml volume,
on a Ferris wheel at 0.3 r.p.m. Clearance and ingestion
rates were calculated after Frost (Frost, 1972).
Once we established the relationship between food
size and feeding rate, we applied it to the five cell size
ranges from our nanoplankton quantifications to calculate an estimate of environmental ingestion rates. We
chose four nanoplankton samples which represented the
lowest, two mid-range, and the highest concentration
among all our samples. The particle concentration in
each of the five cell size ranges was multiplied by the
respective clearance rate for each of the average cell
volumes of the five cell size ranges to obtain the respective ingestion rates.
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Fig. 4. Abundance and vertical distribution of different cell types at four stations.
RESULTS
upper 100 m were lower than off Puerto Rico (casts 11a
and 19).
Hydrography
Particles
At all four stations we encountered a shallow upper
mixed layer which ranged from 10 to 20 m (Figure 2).
Off Puerto Rico (casts 11a and 19), temperature
decreased fairly evenly with depth, reaching near 25.5 C
at 100 m depth, while off the Bahamas the upper part of
the thermocline had a pronounced decrease, which was
followed by a lesser decrease, attaining near 22.5 C at
100 m depth (Figure 2). Salinity increased with depth
from near 36% near the surface to >37% at 100 m
depth off Puerto Rico; off the Bahamas salinity
increased only slightly with depth, from 36.3% to
near 36.5% at 60 m (Figure 2). Chlorophyll profiles
were characterized by a maximum at 110–130 m (Figure 2) with low concentrations from the surface to 40–
50 m, and then increasing towards the maximum. Off
the Bahamas (casts 35 and 41) Chl concentrations in the
We expressed particle concentrations as cells ml1 and
as total cell volume (mm3 ml1), which can be transformed to C by multiplying by 183 mg C mm3 of
particles (Caron et al., 1999). Cells and volumes are
presented logarithmically for better recognition.
First, we present the total nanoplankton abundance
for each depth of each of the four profiles (Table I).
These abundances varied with depth, and also among
casts for the different depths. Friedman’s test comparing
the total particle volumes for each of the upper five
depths (the 140 m sample of cast 35 was lost) among
the four casts revealed that there is no depth at which
particle volume is consistently different from any of the
other four depths in all profiles.
Next we compared the concentration of cells for the
various size ranges (Figure 3). For each cast the sequence
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Fig. 5. Vertical distribution of auto- and heterotrophic cells at four stations.
of cell abundance was 2–4 > 4–6 > 6–8 mm ESD.
Concerning cell type (Figure 4) the sequence of abundance throughout the water column was Pnano >
Hnano > Hdino > Pdino. As to trophic level, autotrophs
were always far more abundant than heterotrophs
(Figure 5). The sharp increase in autotrophs near 120 m
is probably related to the Chl maximum.
For comparative purposes we chose as a common
denominator the total cell volumes for each size range
and also for cell type. An analysis of the cell size range
volumes (mm3 ml1, which can also be expressed as mm3 l1)
versus depth reveals that generally the 10–20 mm ESD
range had the largest volumes (Figure 6). The null
hypothesis that all five cell size range volumes are identical is rejected (Friedman’s test, P < 0.05). The following
multiple comparison test reveals that (Table II): the total
cell volumes in the range 10–20 mm ESD are always the
largest with the ranges 2–4 and 4–6 mm ESD identical
(casts 35 and 41) or being second largest. In three out of
four casts (casts 19, 35 and 41) the range 8–10 mm ESD
had the smallest total volume (Table II; Figure 6).
Concerning total volumes of cell types, we focused on
Pnano, Hdino, Pdino and Hnano because we observed
insufficient numbers of diatoms and ciliates (Figure 7).
The null hypothesis that all four cell types are of the
same total volume at the different depths was rejected
(Friedman’s test, P < 0.05). A multiple comparison test
showed the following (Table III): in all four casts Pnano
and/or Hdino had the largest volumes while Hnano had
the smallest volume, sharing this position with Pdino for
cast 11a (Table III).
We also categorized the volumetric abundance in
relation to trophic level (Figure 8). In three of four
casts, the autotrophs were more abundant at almost all
depths. Off the Bahamas, auto- and heterotroph volumes
occurred at most depths in almost identical concentrations, except those depths near the Chl maximum. Total
abundances decreased with depth in cast 35, but hardly
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Fig. 6. Total volume of cells from five size ranges at four stations.
Table II: Multiple comparison of biovolumes of different cell size ranges following Friedman’s test
(after rejection of the null hypothesis)
Cast 11a
10–20 >
2–4 ¼
4–6 >
8–10 ¼
6–8 mm Ø
Cast 19
10–20 >
4–6 ¼
2–4 >
6–8 ¼
8–10 mm Ø
10–20 ¼
4–6
2–4 ¼
6–8 ¼
8–10 mm Ø
6–8 ¼
8–10 mm Ø
Cast 35
10–20 >
4–6 >
2–4
4–6 >
Cast 41
10–20 ¼
2–4
10–20 >
2–4 ¼
changed with depth for cast 41, except those near the
chlorophyll maxima. The two casts off Puerto Rico
differed widely from each other i.e. in auto- to heterotroph relationships, and also in their vertical distributions (Figure 8).
6–8 ¼
4–6 ¼
8–10 mm Ø
6–8 ¼
4–6 ¼
8–10 mm Ø
Expressing volumetric abundances of the size ranges
as a percentage of the total reveals that the 10–20 mm
fraction usually amounted to between 20 and >50% of
the total (Figure 9). The percent composition of cell size
ranges varied considerably between the casts off the
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Fig. 7. Total volume of cells from four different types at four stations.
Table III: Multiple comparison of biovolumes of different cell types following Friedman’s test
(after rejection of the null hypothesis)
Cast 11a
Pnano ¼
Hdino
> Pdino
Pnano
¼ Hnano
Hdino
¼ Pdino
Hdino
>
Hnano
Pnano
> Pdino
> Hnano
Cast 19
Hdino ¼
Cast 35
Hdino ¼
Pnano
¼ Pdino
> Hnano
Cast 41
Pnano >
Hdino
> Pdino
> Hnano
Bahamas, i.e. 35 and 41. Percentages of cell type volumes
were dominated by Pnano from 25 to near 60%, and
Hdino from near 15 to 60% (Figure 10). The percentage of Hnano in three of four casts decreased with
depth, ranging from 15 to near 5%, and was almost
always the lowest.
Environmental ingestion rates
Lastly, we calculated how much food an adult female of
P. aculeatus would ingest at 20 C at some of the environmental particle abundances as quantified from these four
casts (Table IV). For these calculations we used the
clearance rates obtained for just molted and fertilized
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Fig. 8. Total volume of auto- and heterotrophic cells at four stations.
females of P. aculeatus feeding on phytoplankton cells of a
range of sizes under controlled conditions (see Method).
We chose four environmental samples which represented the lowest, two mid-range, and the highest concentration found in our study (Table I). The amounts
ingested daily ranged from 217 to 2000 ng C (Table IV);
these values would amount to 5.5, 15.8, 23.8 and 50.0%,
respectively, of a female’s body C content of 4.0 mg. The
amounts available in the 10–20 mm ESD range contribute the largest part of the ingested food (Table IV),
ranging from 46 to 82% of total ingested C. This is due
to the clearance rate increasing with particle volume, as
was found empirically with P. aculeatus females (upper
row of Table IV); and to the fact that living particle
concentrations in the 10–20 mm ESD range in the
lower three casts (Table IV) ranged from 38 to 53% of
total nanoplanktonic particle volume. The particulate
matter ingested increased roughly with particle size
range.
DISCUSSION
Hydrography
Our studies occurred in that part of the Atlantic Ocean
which is considered part of the North Atlantic Subtropical
Anticyclonic Gyre, which receives input from both
the North and South Equatorial Currents (Tchernia,
1980; Tolmazin, 1985). The epipelagic water column
in late spring was characterized by a shallow upper
mixed layer, and a thermocline extending to beyond
160 m depth (Figure 2). Our comparative study of two
different locations (Figure 1) revealed differences in the
thermal and salinity structure: off the Bahamas the
upper mixed layer was shallower and the temperature
decrease was more pronounced than off Puerto Rico.
Salinities were near 36% at the surface and exceeded
37% at 120 m off Puerto Rico, the latter being indicative of water originating most likely from subtropical
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Fig. 9. Cell volume as percent of total cell volume for five different size ranges.
Atlantic waters from between 20 and 30 N, and 15 and
55 W [(Tchernia 1980) adapted from G. Schott (Schott,
1944)]. Waters off the Bahamas, although also part of
the Subtropical Gyre, had a different salinity signature,
the salinity hardly changing with depth, being near
36.8% at 40 m depth and deeper. These differences
could be attributed to the variability caused by frequently occurring mesoscale eddies in the subtropical
open ocean [e.g. (McGillicuddy et al., 2001)].
Particles
Detailed quantifications of nanoplanktonic particles
were made by Caron et al. (Caron et al., 1995, 1999),
Dennett et al. (Dennett et al., 1999) and Calbet et al.
(Calbet et al., 2001) in the subtropical and tropical
open ocean. The results of Caron et al. (Caron et al.,
1999) on nanoplankton abundance and distribution
taken from the epipelagial at the JGOFS site off
Bermuda in August 1989 revealed a pronounced upper
mixed layer and a sharp thermocline with near 20 C at
100 m depth, and a Chl maximum between 100 and 120
m. At two of the three stations taken the heterotrophs
and autotrophs had similar abundances at most depths;
e.g. on August 16 autotrophs ranged from 200 to 700
cells ml1, and heterotrophs from 150 to 600 ml1.
The organic C concentrations of the nanoplankton at
these three stations ranged mostly from 0.5 to 5.5 mg
l1 for autotrophs, and from 1 to 7 mg l1 for heterotrophs [(Caron et al., 1999), their fig. 2].
Dennett et al. (Dennett et al., 1999) quantified phototrophic and heterotrophic nanoplankton and several
microplankton components in various parts of the
Arabian Sea during the north-east monsoon (NE monsoon) and the spring intermonsoon (SI monsoon) period.
We focused our attention on offshore stations S11 and
S15, from which detailed vertical profiles were obtained.
During the NE monsoon, abundances of both auto- and
heterotroph nanoplankton were similar and hardly
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Fig. 10. Same as Figure 9 but for different cell types.
changed with depth, being near 150–400 cells ml1 for
each. During the SI monsoon period, autotrophs outnumbered heterotrophs at almost every depth. The average auto- and heterotrophic nanoplankton biomass at
three offshore stations (S11, 13 and 15) over the upper
160 m ranged from 2.8 to 4.7 mg C l1 for the former,
and from 3.1 to 4.5 for the latter during the NE
monsoon; and from 2.7 to 3.4 mg C l1 for the former,
and from 1.7 to 2.0 for the latter during the intermonsoon period (SI monsoon).
Calbet et al. (Calbet et al., 2001) quantified the abundance and size distribution of heterotrophic flagellates
(Hflag), and the abundance of autotrophic flagellates
(Aflag) in oceanic waters off Hawaii at different times
of the year in different depth layers. They included cells
<2 mm ESD in their counts. In their four mixed layer
samples, Hflag biomass exceeded that of Aflag, the former ranging from 12 to 21 mg C l1, and the latter from
6.5 to 10 mg C l1. Hflag <2 mm ESD, despite amount-
ing to 30–50% of all cells, contributed on average not
more than 10% of the Hflag biomass. Of four size
categories (2–4, 4–5, 5–10 and >10 mm ESD), the latter
accounted for near 50% or more of the total Hflag
biomass, which in three out of four stations was followed
by that of 2–4 mm ESD.
Comparing the data of these three groups of authors
with ours reveals the following: the average total amount
of nanoplankton did not vary much between the Sargasso
Sea, Arabian Sea and the subtropical/tropical Atlantic
(Table V). The results from Calbet et al. (Calbet et al.,
2001) for the tropical Pacific originated from a wider size
range. However, they are included because we would like
to illustrate the abundance relationships between autoand heterotrophs: Calbet et al. (Calbet et al., 2001) found
nearly three times more hetero- than autotroph biomass,
while from the other regions there was no diffference
between the two, or only slightly higher auto- than heterotroph biomass. In our study we observed pronounced
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Table IV: Paracalanus aculeatus female: daily ingestion rates at environmental food concentrations
at 20 C
ESD (mm)
2–4
4–6
9
29
6–8
8–10
10–20
Total
99
177
–
Clearance rate
(ml female1 day1)
57
Cast 41, 45 m
Particle conc. (mg C l1)
0.85
0.67
0.89
0.38
0.57
3.36
Ingestion
(ng C female1 day1)
8
19
51
38
101
217
Cast 11a, 105 m
Particle conc. (mg C l1)
1.44
1.23
0.68
0.82
2.61
6.78
Ingestion
(ng C female1 day1)
13
36
39
82
461
631
Cast 35, 75 m
Particle conc. (mg C l1)
1.26
1.40
0.74
1.35
4.10
8.86
Ingestion
(ng C female1 day1)
11
40
42
134
726
953
Cast 35, 105 m
Particle conc. (mg C l1)
1.70
2.90
2.47
1.22
9.27
17.56
Ingestion
(ng C female1 day1)
15
84
140
121
1640
2000
The upper row shows the clearance rates by which the particle concentrations were multiplied to obtain the ingestion rates.
Table V: Average abundances of auto- and heterotrophs in subtropical/tropical open ocean regions (g C l1)
Autotrophs
+
Heterotrophs
¼ Total
Reference
4.7
+
4.3
¼ 9.0
Caron et al., 1999
3.5
+
3.5
¼ 7.0
Dennett et al., 1999
¼ 4.8
Dennett et al., 1999
NE Monsoon
3.0
+
1.8
SI Monsoon
8.3
+
(Aflag)
5.6
¼ 24.5
16.2
(Hflag)
+
Calbet et al., 2001
Mixed layer
¼ 9.3
3.7
This study
2–20 mm ESD by Caron et al. (Caron et al., 1999) and Dennett et al. (Dennett et al., 1999), and this study; <2 to >10 mm ESD by Calbet et al. (Calbet et al.,
2001).
similarities in the biovolume of auto- and heterotrophs off
the Bahamas (casts 35 and 41, Figure 8) but differences in
the absolute volumes between the two casts. The two casts
off Puerto Rico (casts 11a and 19) differed widely as to
abundance and vertical distribution of auto- and heterotrophs amongst themselves and within.
Previously published data on size distributions within
the nanoplankton are few. We recalculated the Hnano
biovolumes for the August samples of Caron et al.
[(Caron et al., 1999), their fig. 7] and found that of
ranges 2.2–4.0, 4.0–5.8, 5.8–7.4 and 7.4–10.0 mm
ESD, the first had the smallest and the last the highest
biovolume, ranging from 2700 to 9500 mm3 ml1. In
our studies the 8–10 mm ESD biovolume (auto- and
heterotrophs together) always had the lowest value as
compared with the other four range, of which the 10–20
mm range was always the largest (Table II). Either the
2–4 or the 4–6 mm range had the second largest values,
indicating that the total volumes of smaller diameter cell
ranges are higher than those of larger diameter cell ranges,
as long as cell diameter ranges are identical [Table II
(Sheldon et al., 1972)].
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In our study we extended the differentiation amongst
auto- and heterotrophs by separating flagellates from
dinoflagellates (Figures 4 and 7). Whereas Pnano outnumbered Hnano by a large margin, the Hdino were
always more abundant than the Pdino. In general,
Hnanos were smaller than Pnanos, and Hdinos smaller
than Pdinos. Most Hnanos were <2 mm ESD, and most
Pdinos >20 mm ESD (M. Tzeng, personal communication). Whereas the total volume of Pnanos and Hnanos
decreased with cell size, that of Pdino and particularly
Hdino increased with cell size. Repeatedly the ranges 6–
8 and 8–10 mm ESD had similar volumes per milliliter,
which were always surpassed by the 10–20 mm range
volumes. It appears that most of the autotroph biomass
was in the smaller ranges, and that of the heterotrophs in
the larger ones.
Environmental ingestion rates
The daily ingestion rates calculated for females of the
calanoid P. aculeatus at 20 C (Table IV) ranged from 5.5
to 50.0% of the female’s body weight/C. At the near
average particle concentration of 8.86 mg C l1 a female
would ingest 23.8% of its body C. To what extent would
that rate cover its metabolic expenditures, and possibly
reproduction? Applying Ikeda’s regression on oxygen consumption versus copepod body C content [(Ikeda, 1985),
his table 3] resulted in a daily energy consumption of
12.7% of the body content of 4.0 mg C (P. aculeatus
female); we related 1 ml of oxygen consumption = 4.82
cal (Winberg, 1971), and 1 mg of copepod dry weight =
5.0 cal. At 70% assimilation efficiency, which is usually
applied for ingested phytoplankton, the copepod would
have to ingest daily 18.1% of its body C just for basal
metabolism. If, however, we apply 90% assimilation
efficiency (Conover, 1979), then this copepod would
need to ingest only 14.1% of its body C daily. According
to Conover (Conover, 1979), animal tissue is assimilated
at a much higher rate than plant tissue in the planktonic
environment. Since most of the P. aculeatus female’s ingestion would originate from particles 10–20 mm ESD
(Table IV), which are mostly heterotrophs (Tables II and
III, most of the Hdino total volume being in the 10–20 mm
range), we could assume a >70% assimilation efficiency;
also, the overall very low food concentrations lead to
extended gut residence times, which again should increase
assimilation efficiency. In essence, at a particle concentration of 8.86 mg C l1, with its observed particle size
distribution, this copepod would have assimilated 858 ng
of the 953 ng C ingested C at 90% efficiency (Table IV).
After subtracting 508 ng C for basal metabolism, the
female would have 350 ng C available for other purposes
e.g. enhanced metabolism, and reproduction. The sig-
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nificance of ingesting heterotrophs to meet the oceanic
copepods’ food demands was emphasized by Roman and
Gauzens (Roman and Gauzens, 1997).
At the food concentrations and their size distributions
given here (e.g. Table IV), a P. aculeatus female would
require, applying the given clearance rates (Table IV), at
least a nanoplankton concentration of 5.3 mg C l1 to
cover its basal metabolism. Concentrations in excess of
that value were found at all depths except two (Table I).
To account for the effects of higher temperatures,
enhanced metabolism and reproduction, concentrations
in excess of 8 mg C l1 are most probably needed for
an adult female of P. aculeatus. The previous calculations
should be considered only towards requirements of feeding-current producing calanoid adult females, and not
for their nauplii or early to mid-copepodid stages. Also
not for Clausocalanidae, Cyclopoida and Poecilostomatoida which have different feeding behaviors and metabolic requirements.
Eventually we will analyze field observations on the
ingestion of various sizes and types of food by oceanic
calanoids, interpret those observations with food abundances and distributions reported here, and then present
an in-depth evaluation of the probability of copepods
existing in a truly ‘nutritionally-dilute environment’
(Conover, 1968). One important aspect will be the quantification of feeding rates of juveniles of different abundant copepod species on the range of available particle
sizes and types. The fact that the stage durations of
various copepod species increased from copepodid
stage I towards older copepodids [(Webber and Roff,
1995b), their table 4] could be an indication of the effect
of increasing cell volume per milliliter concentrations
(increasing food abundance) with decreasing cell ESD,
despite increasing specific metabolic rates with decreasing copepod size.
ACKNOWLEDGEMENTS
This research was supported by NSF Grant OCE
99 11513. We would like to thank the captain and
crew of the R/V ‘Cape Hatteras’ and the Marine Superintendent of the Duke University Marine Laboratory for
their can-do attitude and professional cooperation. We
would also like to thank Dr A. Calbet for providing data,
Dr P. G. Verity for letting us use his optics facilities, and
Anna Boyette for preparing the figures.
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Received on May 8, 2003; accepted on August 28, 2003
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