JournaJ of Plankton Research Vol.18 no.l pp.87-95,1996
Conservative features of picoplankton in a Mediterranean
eutrophic area, the Bay of Naples
M.Modigh, V.Saggiomo and M.Ribera d'Alcala
Laboratory of Biological Oceanography, Stazione Zoologica, Villa Comunale,
1-80121 Naples, Italy
Abstract. Autrophic picoplankton abundances and production are reported for a Mediterranean
coastal study site. The presence of a relatively stable picoplanktonic compartment in a eutrophic highly
variable area is discussed.
Introduction
The Gulf of Naples (Mediterranean Sea) is deeper (mean depth —150 m) than
most coastal embayments and is strongly coupled with open Tyrrhenian waters for
most of its area, extending over the continental slope. However, its inner part, the
Bay of Naples, receives untreated urban wastes and is subjected to irregular pulses
of fresher nutrient-enriched waters, resulting in eutrophication. No stable frontal
structure has been observed between these two areas of the Gulf.
A fixed station (MC), located in the boundary region, has been sampled for
hydrographical and biological (phyto- and zooplankton) parameters since January
1984. Phytoplankton blooms were observed during all seasons (Marino etal., 1984;
Zingone et al., 1990) and primary production, measured from 1984 until 1988, at
MC was 234 ± 318 g C nr2 year1. On the other hand, zooplankton populations
showed a repetitive pattern of succession over the years of study with the annual
zooplankton maximum occurring in midsummer when very low phytoplanktonic
biomass was generally recorded (Scotto di Carlo et al., 1985; Mazzocchi and Ribera
d'Alcala, 1995). This observation was one of the stimuli to study the autotrophic
compartment in more detail.
The importance of autotrophic picoplankton in all aquatic systems is well documented (for reviews, see Joint, 1986; Stockner, 1988). In oligotrophic areas, picoplankton contribute up to 90% of phytoplankton biomass, whereas lower
contributions, <30%, are recorded in coastal waters. The object of the present
study was picoplankton dynamics during an annual cycle at station MC.
Method
The site has been sampled biweekly since January 1984 at 10 depths with 51 Niskin
bottles, fitted with reversing thermometers. Temperature and salinity were also
obtained from a CTD profiler (Idronaut 901). Inorganic nutrients and photosynthetic pigments were analyzed by standard methods (Scotto di Carlo et al., 1985).
Zooplankton net tows, 50-0 m, 200 u,m mesh size, were also made. Incident solar
radiation was registered with a Licor 550B Printing Integrator.
© Oxford University Press
87
M.Modigh, V.Saggiomo and M.Ribera d'Alcala
From May 1988 until May 1989, picoalgal cell numbers and biomass (chlorophyll
a) were measured biweekly at four depths: 0, 5, 10 and 40 m. Inorganic carbon
assimilation was determined from May until December 1988.
For cell counts, duplicate subsamples of 20-50 ml were passed serially through
Nuclepore membranes of 2,1 and 0.22 p.m pore size,rinsedwith 10 ml autoclaved,
pre-filtered (0.22 u,m) seawater, in order to avoid cells being retained within the
detritus filaments. Counts were performed immediately with a Zeiss epifluorescence microscope. Epifluorescence microscope observations showed that after
careful rinsing, virtually no cells were retained on the 2 u,m membranes, while a
variable percentage (0-94%) of the picoplanktonic algae were retained within
detritus filaments on the 1 u,m membrane. Total cell numbers were obtained adding the counts of the serial filtration of each sample onto 1 and 0.22 pore size
membranes.
For chlorophyll a and pheopigment measurements, subsamples of 100-200 ml
were filtered onto Nuclepore membranes of 2 ^.m pore size (rinsed as above) and
Whatman GF/F filters, extracted overnight in neutralized acetone and fluorescence determined with a Turner 111 Fluorimeter (Yentsch and Menzel, 1963).
For inorganic carbon assimilation measurements, samples were passed through
a 150 u.m mesh size net, poured into 300 ml BOD bottles (two light, one dark) and
10 JJLQ Na2HCO3 were added. Incubations were carried out for 4 h around noon at
depth. Subsamples from each incubation bottle were filtered as described for the
fluorimetric measurements.
Results
The thermocline, formed in early April, was at —15 m depth in May, going progressively deeper during summer to ~40 m in October, then disappearing completely from November until March. The maximum annual temperature was
27.8°C at the surface, while the minimum winter temperature for the whole water
column was 13.98°C in March 1989. The salinity values were generally within the
range 37.8-38.2 PSU, with scattered, lower values down to 36.8 PSU at the surface.
Inorganic nutrient concentrations showed strong fluctuations: total inorganic
nitrogen (TIN): 0.85 ± 1.50 \imol N dm"3; N = 420 and phosphate: 0.35 ± 0.37
jjuinol P dm"3; N = 140. However, TIN and phosphate always exceeded 0.51 u,mol N
dm"3 and 0.23 nmol P dnr3, respectively. The lowest nutrient concentrations were
recorded in July-August.
Total daily irradiance varied from 1.35 E nr 2 day-' (December) to 49.61 E nr 2
day 1 (July). Average daily irradiance was calculated for the 2 weeks preceding
each incubation experiment, the lowest variation in incident light was recorded for
the period 20 July-3 August, 35.96 ± 1.04 E nr 2 day-1 (Figure 1).
Picoplankton cell concentrations ranged from 1.6 to 69.3 x 10* cells dm"3 (average 14.38 ± 13.54 x 106). Highest values were registered in summer with maximum abundances for all four depths observed on 3 August (Figure 2a and b). The
three samples collected within the 0-10 m layer showed similar oscillations of cell
concentrations as long as the stratification persisted. From the end of October,
88
Picoplankton dynamics in Bay of Naples
30
15
O
Fig. 1. Average temperature in the 0-10 m layer and daily irradiance, averaged for the 2 weeks preceding each sampling date, May until December 1988 at MC.
with the breaking down of the thermocline, a homogeneous distribution of picoplankton cell concentrations was observed.
The major part of the population was yellow-fluorescing cyanobacteria of Synechococcus type, 0.5-1.5 p.m in diameter. Looping motility was observed in some of
these cells. Red-fluorescing, eukaryotic cells of 1-2 u.m diameter made up an average of 3.4% of the total picoplankton population. Highest numbers (>106 cells
dnr3) and percentages, up to 20%, were observed in the two November samplings.
Very small, <0.5 \im, red-fluorescing cells were observed occasionally, but in great
numbers. The method used did not allow us to count these very small cells.
Phytoplankton biomass varied between 0 and 4.96 (xg chl dm"3 (average
1.05 ± 1.28) for the >2 jxm fraction, and between 0 and 0.54 |xg chl dm"3
(0.18 ± 0.15) for the <2 |xm fraction, in the 0-10 m layer. At times, when total
chlorophyll concentrations were below 1 (xg dm 3 , the <2 u,m fraction accounted
for up to 100% of chlorophyll a values.
Carbon assimilation values in the 0-10 m layer showed higher values and more
pronounced oscillations for the >2 jxm fraction (Figure 3a), as compared to the
picoplankton fraction (Figure 3b). Highest values were observed at 0 m
(14.93 ± 13.96; maximum 32.53 jxg C dm 3 Ir1) for the >2u,m fraction and at 5 m
(1.97 ± 1.2, maximum 3.68 jig C dm"3 h~') for the <2 (xm fraction. The decline in
carbon assimilation with depth was much steeper for the >2 u,m fraction as compared to the picoplankton fraction. Figure 3c shows depth-integrated primary production; the picoplankton contribution amounted to 27% of total primary
production for the period studied.
Figure 4 shows integrated (0-60 m) values for total chlorophyll a concentrations
from 1984 to 1989 at station MC. Oscillations were very sharp with the lowest
values in midsummer and winter, but an average chlorophyll a concentration of <1
jxg chl dm"3 was frequently observed over all seasons.
Seasonal variations in zooplankton biomass and abundances repeated the same
annual pattern over this 6 year period, with the lowest values observed in winter
89
M.Modigh, V^aggiomo and M.Riben d'Alcatt
M
J
J
A
S
O
N
D
J
F
M
2000
A
M
2500
8
M
A
M
Fig. 2. (a) Picoalgal cell abundances at four depths; (b) integrated picoalgal cell abundances in the 0-40
m layer (solid line) and P.avirosiris abundances (dotted line), May 1988 until May 1989 at MC.
and the highest in midsummer. Copepods were the most abundant group, but the
annual zooplankton summer maximum was mainly due to the rapid increment of
cladocerans, with Penilia avirostris being by far the most dominant species (Mazzocchi and Ribera d'Alcala, 1995; M.G.Mazzocchi, personal communication).
Discussion
The relative stability of picoplankton parameters differed markedly from the pronounced variability experienced in the area.
Cell concentrations were fairly stable throughout the year, oscillations being
less than one order of magnitude, while variations over two or three orders of
magnitude have been reported for inshore Mediterranean (Revelante and Gilmartin, 1988; Vanucci et al., 1994) and other coastal areas (Waterbury et al., 1986;
Kuosa, 1991).
Our data fit well within the range reported for other Mediterranean sites for
picoalgal abundances (Zaika, 1986; Magazzu et al., 1987; Li et al., 1992; FerrierPages and Rassoulzadegan, 1994) and chlorophyll concentrations (Raimbault
90
Picoplankton dynamics in Bay of Naples
M
250
Fig. 3. Inorganic carbon assimilation (a) for the >2 nm fraction; (b) for the <2 (im fraction; (c) integrated for the 0-40 m layer for both fractions, May until December 1988 at MC.
91
M.Modlgh, V.Saggiomo and M.Ribera d'Akala
250
1984
1985
1986
1987
1988
1989
Fig. 4. Integrated (0-60 m) chlorophyll a concentrations at MC, 1984-1989. The horizontal line indicates an average concentration of 1 fig chl dm3.
etal., 1988; Vanucci etal., 1994). The 27% picoplankton contribution to total phytoplankton production was within the range reported for a Southern Tyrrhenian
site (Magazzu et al., 1987) and other coastal areas (Joint et al., 1986; Sherr et al.,
1986; Stockner and Antia, 1986).
The picoalgal community was dominated by small (~1 u,m) Synechococcus,
while enlarged cells (1.4-2.2 ^m) reported from other coastal areas (El Hag and
Fogg, 1986; Jochem, 1988) were not observed. Another indication of the openwater character of the picoalgal community, besides the concentrations and the
small cell size, was the presence of some Synechococcus showing looping motility
which, to our knowledge, has been reported only in open-ocean areas (Waterbury
et al., 1985,1986).
We presume the tiny red-fluorescing cells to be Prochlorococcus, as indicated
both by their small dimension and the rapidly fading fluorescence which make
microscope counting unfeasible (Campbell et al., 1994).
The major importance of the picoplankton contribution was observed when
total phytoplankton biomass was low, ^lu-g chl dm \ a condition frequently
observed at the study site. Oscillations for chlorophyll a and primary production
measurements were less pronounced in the picoplankton fraction than those registered in the >2 ^.m fraction. A lack of correspondence was observed between picoplankton cell abundances and chlorophyll and carbon assimilation values; the
same mismatch has been reported elsewhere (Jochem, 1988; S0ndergaard et al.,
1991; Andersson et al., 1994), but it still remains an open question.
No connection was evidenced between variations in salinity and picoalgal abundances. Furthermore, the annual picoalgal peak occurred in summer when the
lowest nutrient concentrations were recorded.
Picoplankton production, in particular when integrated for the water column,
matches the irradiance as well as the temperature curve (Figures 1 and 3c). However, since temperatures over 10°C have not been shown to further enhance picoplankton production (Andersson et al., 1994), we presume light availability and
perhaps light history to be more important, as suggested by Murphy and Haugen
(1985). The low variability in daily irradiance recorded for the 2 weeks preceding
92
Picoplankton dynamics in Bay of Naples
the picoplankton peak is typical for the midsummer period and might well contribute to the picoplankton maximum frequently observed in temperate regions in
that period (Joint et al., 1986; Jochem, 1988; Vanucci et al., 1994).
The autotrophic picoplankton show annual variations of two or three orders of
magnitude in coastal areas because of low temperatures inhibiting growth (Waterbury et al., 1986; Jochem, 1988), nutrient (nitrogen) limitation (Ferrier-Pages and
Rassoulzadegan, 1994; Vanucci et al., 1994) or light limitation (Kuosa, 1991). In the
Bay of Naples, in the absence of particular environmental constraints, such as low
temperatures, nutrient depletion or too short days, the picophytoplankton might
be predominantly grazer controlled.
The peak observed in picoplankton cell numbers in August was coincident with
the annual zooplankton maximum, due to a >10-fold increase in the cladocerans.
The cladoceran maximum persisted from the end of July through September:
1804 ± 732 ind. nr3, N = 5, while abundance for the five samplings preceding this
peak was 162 ± 71 ind. nr3. The dominant species P.avirostris has been reported
not to feed on picoplankton, but to feed on smallflagellates,which in turn graze
picoplankton (Turner et al., 1988). We hypothesize that an increased grazing pressure on the flagellates by the emerging cladocerans might result in a temporary
release of grazing pressure on the picoplankton. As reported by Kuosa (1991), the
flagellate growth rates indicate their ability to keep pace with their picoplanktonic
food sources. This could explain the picoplankton concentrations returning to
usual levels by mid-August while cladoceran abundances remain high until the end
of September at station MC. The picoplankton peak would thus be due to accumulation rather than a real increase in production. Sherr et al. (1986), discussing the
(unknown) fate of picoplanktonic production, affirmed that accumulation never
occurs. However, Weisse (1991) observed an accumulation of bacterioplankton
due to a peak in ciliate abundances, which in turn grazed the heterotrophic flagellates normally controlling bacterial numbers.
If the midsummer peak was due to the lack of grazing, then the difference
between the production peak and the normal levels of measured production might
give an indication of the amount of picoalgal production constantly removed. Correcting for cell abundances and light availability, we calculated 152.8 mg C nr 2
day 1 of unseen (grazed) production. Although the estimate is very rough and no
data are available as to the real contribution to higher trophic levels, the presence
of a fairly constant, reliable resource might have a stabilizing effect on the system
as a whole, also suggested by the repetitive annual pattern of the zooplankton
populations.
In the Bay of Naples, notwithstanding strong eutrophic signals such as low salinity inputs, nutrient pulses, frequent phytoplankton blooms and a high primary
productivity, the picoplankton compartment seems to maintain an 'oligotrophic
character', as outlined above. The microbial compartment, although making a
minor contribution to total production, is also important in coastal areas (Sherr et
al., 1986), perhaps supplying a stable background in the coastal pelagic system.
Acknowledgements
We thank Dr M.G.Mazzocchi for providing her unpublished zooplankton data and
for helpful criticism of the manuscript.
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M.Modigh, V.Saggiomo and M.Ribera d'Akala
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Received on May 16, 1995; accepted on September 25, 1995
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