Download STOCKNER, JOHN G. Phototrophic picoplankton

Limnol. Oceanogr., 33(4, part 2), 1988, X5-775
0 1988, by the American Society of Limnology
and Oceanography,
Phototrophic picoplankton:
freshwater ecosystems
Inc.
An overview from marine and
John G. Stockner’
Canada Fisheries and Oceans, West Vancouver
West Vancouver, British Columbia V7V lN6
Laboratory,
4160 Marine
Drive,
Abstract
Algal picoplankton are a ubiquitous component of the microbial plankton communities of both
marine and freshwater ecosystems. They contribute significantly to the total biomass of phytoplankton communities, and in oligotrophic oceans and lakes can be responsible for up to 80-90%
of the total daily or annual carbon production. As part of the “microbial
loop,” they are thought
to be grazed by flagellates, ciliates, rotifers, copepods, and other metazoans, and contribute to the
flow of energy to higher trophic levels. This presentation highlights their discovery, distribution,
physiology, production, and contribution
to pelagic food webs in marine and freshwater systems.
The discovery of minute (0.2-2.0 pm)
phototrophic picoplankton in the late 1970s
in great abundance in both marine (Johnson
and Sieburth 1979; Waterbury et al. 1979)
and freshwater (Paerl 1977) ecosystems led
to a resurgence of research activity worldwide. Many investigators believed this discovery provided the “missing link” in the
controversial carbon supply/demand question in the world’s oceans (Sorokin 197 1;
Banse 1974; Johnson et al. 198 1) and that
it added credibility to the emerging new paradigm that focused on the significance of
microbial food webs in energy transfer, carbon recycling, and nutrient release in aquatic ecosystems (Pomeroy 1974; Azam et al.
1983; Williams 1984; Caron et al. 1985a).
The literature on the occurrence and distribution,
photosynthesis and physiology,
and production and ecology of algal picoplankton is already quite extensive, and the
subject has only recently received a comprehensive multidisciplinary
review (Stockner and Antia 1986). The basic purpose of
this presentation is to provide a general
overview of key findings from the literature,
most notably those pertaining to the discovery, taxonomy, physiology, and ecology
of algal picoplankton
in both marine and
’ I dedicate this overview to Dr. N. J. Antia on the
occasion of his retirement from Canada Fisheries and
Oceans, West Vancouver Laboratory, in February 1986.
The invaluable support and inspiration of Dr. Antia
led to the comprehensive
picoplankton
review of
Stockner and Antia (1986) and to other, numerous
contributions
to the field of phycology.
freshwater systems. This overview focuses
on photoautotrophic
(algal) picoplankton
and follows the terminology and logical size
boundaries for pelagic plankton as defined
by Sieburth et al. (1978): microplankton (20200 pm), nanoplankton (2-20 ,um), and picoplankton (0.2-2 pm).
Occurrence and discovery
Before the joint discovery of chroococcoid cyanobacterial ubiquity in the oceans
by Johnson and Sieburth (1979) and Waterbury et al. (1979) there were only incidental reports of small, picoplankton-sized
cyanobacteria and chlorophyceans in both
marine and freshwater ecosystems (Fig. 1).
Since 1982, the number of reported algal
picoplankton occurrences has risen sharply,
and at present, with the exception of the
Black and Red Seas, they have been discovered in all the major oceans of the world
(Fig. 2). In lakes, the major discoveries have
come from Europe, North America, and
New Zealand (Fig. 2). They have apparently
not yet been studied in lakes from Africa,
South America, Japan, or Australia, and,
apart from the reported occurrence of picosized algae in Lake Baikal (Votintsev et al.
1972), no accounts of their presence in Asian
lakes are known.
Enumeration and taxonomy
There are two major groups of algal picoplankton divisible by cellular structure:
procaryotic (cyanobacterial) and eucaryotic.
The recognition
of cyanobacterial
picoplankton was facilitated by the application
765
St&liner
Throndsen
(1978)
Munawar
Fig. 1. Chronology
of discovery
of minute algal picoplankton
of epifluorescence microscopy adapted from
its initial development for the enumeration
of heterotrophic bacteria (Hobbie et al. 1977;
Daley 1979). No fluorochrome
stains are
necessary for their enumeration
because
each cyanobacterial
picoplankter
has a
unique autofluorescent
spectral signature,
usually distinguishable from eucaryotic pi-
Fig. 2.
Geographic
occurrence
of algal picoplankton
in marine and freshwater
& Fahnenstiel
(1982)
ecosystems.
coplankton because of their red autofluorescence emitted by chlorophyll. However,
some phycocyanin-rich
cyanobacteria have
emission and excitation wavelengths that
may not be visually distinguishable
from
red fluorescing chlorophyll. If complete separation of major algal picoplankton groups
is required, an indirect immunofluores-
reported thus far in marine and freshwater
ecosystems.
Phototrophic picoplankton
cence technique may have to be used (see
Campbell et al. 1983).
Because of their extremely small size, it
is likely that the ultimate identification
of
autotrophic picoplankton will require ultrastructural
examination
by transmission
electron microscopy (TEM). In fact, it was
TEM examination that provided our first
observations of the occurrence of eucaryotic
as well as procaryotic marine picoplankton
(Johnson and Sieburth 1982).
Apart from their enumeration by epifluorescence microscopy, which enables a preliminary separation into eucaryotic and cyanobacterial
groups, surprisingly
little
taxonomic work has been done. Because of
the overall difficulty of unequivocal idcntification of cyanobacteria and the greater
reliance placed on assigning numbers to new
isolates, Griffiths (1984) has only recently
devised a descriptive nomenclature system
for these microorganisms.
I have listed in
Table 1 some preliminary
picoplankton
identifications from marine and freshwater,
along with the investigator(s) who first mentioned, discovered, or obtained them in field
collections
and/or subsequently
isolated
them in laboratory cultures.
Pigments, photosynthesis, and nutrients
The major photosynthetic
pigments of
chroococcoid
cyanobacteria
reported by
several investigators are listed in Table 2.
Chlorophyll a is the only known chlorophyll
from these microorganisms
(Stransky and
Hager 1970), and zeaxanthin is the dominant carotenoid pigment. Guillard et al.
(1985) have suggested that zeaxanthin may
be a useful picoplankton marker, at least in
the marine environment.
A considerable
amount of work has been done on the physiology and biochemistry
of phycobiliproteins of chroococcoid cyanobacteria, most
recently on clones of the picoplankter Synechococcus(Alberte et al. 1984; Wood et al.
1985). There is a strong preponderance of
chroococcoid
cyanobacteria picoplankton
rich in phycoerythrin
(PE) in tropical and
temperate oceanic and offshore marine regions throughout the year (Waterbury et al.
1979; Glover et al. 1985b). These PE-rich
cyanobacteria have developed chromatic
adaptation to the quality and intensity of
767
- Table 1. Procaryotic and eucaryotic picoplankton
from marine and freshwater ecosystems.
Procaryote
Cyanobacteria
Chroococcales
Marine
Synechococcus (Johnson and Sieburth
Waterbury et al. 1979)
Synechocysti.s (Campbell et al. 1983)
1979;
Freshwater
Cyunodictyon reticulaturn (Cronberg and
Weibull
198 1)
Cyanonephrori styloides (Hickel 198 1)
Synechococcus (Drcws et al. 1961)
Eucaryotc
Chlorophyccae
Marine
Chlorella-like
(Johnson and Sieburth 1979;
Joint and Pipe 1984; Takahashi and
Hori 1984)
Chlorella nana (Andreoli et al. 1978)
Nannochloris spp. (Butcher 1952; Sarokin and
Carpenter 1982)
Freshwater
Chlorella minutissima (Fott and Novakova
1969)
Stichococcus spp. (Butcher 1952; George
1957)
Prasinophyceae
Marine
Micromonas pusilla (Johnson and Sieburth
1982)
Pyramimonas spp. (Takahashi and Hori 1984)
Dolichomastix lepidota (Manton 1977)
Eustigmatophyceae
Marine
Nannochloropsis spp. (Turner and Gowen
1984)
Bacillariophyceac
Marine
“unidcntificd”
(Takahashi
and Hori
1984)
Cryptophyccac
Marine
Ifillea marina (Butcher 1952)
Freshwater
Rhodomonas pygmaea (Javornicky
1976)
Others
“unidentified
chrysophytes”
(Takahashi and
Bienfang 1983)
“unidentified
haptophyte”
(Takahashi and Hori
1984)
768
Stockner
light available at the oceanic depth where
they normally occur (Wood 1985). Another
interesting adaptive feature of marine Synechococcus is their ability to saturate photosynthesis and growth rate at very low irradiances (Morris and Glover 198 1). This
finding is consistent with the first observations of their maximum abundance at or
near the base of the euphotic zone in coastal
and offshore marine waters (Glover 1985;
<ilover et al. 1986; Putt and Prezelin 1985).
The chlorophyll pigment composition of
eucaryotic picoplankton (Chl a + b, or a +
c) is thought to be responsible for their predominance at the 0.5% light level, below
the peak of Synechococcus populations
(Glover et al. 1986). The eucaryotic pigment composition
confers greater growth
and photosynthetic
efficiencies in the dim
blue-violet light at the base of the euphotic
zone, while PE-rich Synechococcus cells are
favored by green light at the 1% level.
Under culture conditions, some major picoplankters have shown the ability to survive and resume growth after periods of total darkness (Antia and Cheng 1970; Antia
1976). Such a pronounced capacity for survival in the dark would enable them to survive the seasonal rhythm of winter darkness
and the sinking into the aphotic zone. This
viewpoint has recently been supported by
Platt et al. (1983b), who found photosynthetically
competent
phytoplankton
at
1,000-m depth in the eastern tropical Pa-
pulses of elevated nutrient concentration
exist. Evidence for such pulsing has been
reported for oceanic regions (Holligan et al.
1985; Jenkins and Goldman 1985), but not
yet for lakes.
Marine picoplankton are capable of utilizing nitrate, ammonium, and urea as sole
nitrogen sources for growth, but Probyn
(1985) and Probyn and Painting (1985) have
reported that picoplankton of < 1.O-pm size
in the southwest Atlantic and in Antarctic
waters showed a preference for reduced nitrogen in the form of ammonium or urea.
In the same study, they found that picoplankton accounted for about 80% of the
nitrogen uptake by the total phytoplankton
community in oceanic stations but only 50%
in offshore stations close to the ice edge
(Probyn and Painting 198 5). Picoplankton
can also use various sources of organic nitrogen (Neilson and Larsson 1980), and
cyanobacterial
picoplankton
appear able
to utilize their phycocyanin as a nitrogen
reserve under conditions of severe N deprivation (Antia and Cheng 1977). It also
appears that at least some freshwater chroococcoid cyanobacteria are capable of N2 fixation (Wyatt and Silvey 1969; Rippka et al.
1979). Virtually all N2 fixers originated in
fresh or brackish waters, but, as yet, no observations of N2 fixation by oceanic Synechococcus or Synechocystis have been reported.
cific.
Primary production and bimoass
Because of their extremely small size, algal picoplankton
have very rapid nutrient
uptake rates (Friebele et al. 1978; Lehman
and Sandgren 1982; Suttle and Harrison
1986). Although
Lehman and Sandgren
(1982) reported a short-lived (few minutes)
sustainability of the high uptake rate, Suttle
and Harrison (1986) using Synechococcus
from a coastal British Columbia lake showed
little or no reduction of the uptake rate per
cell in response to increasing cellular-P over
a period of at least 100 min. If the latter
observation is found to be widespread and
typical of Synechococcus in both freshwater
and marine systems, then the ability to sustain high uptake rates while cell quota is
rapidly increasing should confer competitive advantage in areas where ephemeral
Table 3 summarizes published estimates
of photoautotrophic
picoplankton
growth,
production, and biomass from both freshwater and marine ecosystems. Hourly carbon production rates for marine picoplankton ranged from a low of 0.01 mg C m-I’
h-l reported by Saijo and Takesue (1965)
to over 3 1 mg C rnh3 h-l observed by Glover et al. (1985a). The percentage contribution by picoplankton
to total carbon production ranged from 1 to 90%, with a
tendency for substantially higher contributions in more oligotrophic
regions of the
world’s oceans. Estimates of algal picoplankton biomass (chlorophyll)
were generally less variable than production, ranging
from 0.05 to 1.0 mg Chl m-3, and contributing from 1 to 90% to total chlorophyll
Phototrophic picoplankton
biomass. Reported assimilation
numbers
(AN) for algal picoplankton were quite high,
with values ranging from 0.3 to 14.5, indicative of a rapid turnover of carbon per
unit chlorophyll.
There were fewer measurements of specific growth rates (p) reported, but values, ranging from 0.15 to 8.9
d-l, tended to be considerably higher in upwelling and neritic regions than in tropical
and subtropical oceans (Li et al. 1983; Landry et al. 1984).
Rates of picoplankton carbon production
from freshwater are lower than marine values, ranging from 0.1 to 7.0 mg C m-3 h-l,
representing 16-70% of total carbon production (Table 3). Chlorophyll
biomass of
algal picoplankton contributed 6-43% to total phytoplankton
chlorophyll, with values
ranging from 0.3 to 1.O mg Chl m-3. Specific
growth rates have been determined on cyanobacterial picoplankton in Lake Superior, and for September 1983 were 1.5 d-l in
the epilimnion and 0.8 d-l in the hypolimnion (Fahnenstiel et al. 1986). Assimilation
numbers reported by Costella et al. (1979)
and Munawar and Fahnenstiel(l982)
were
similar, ranging from 2.0 to 2.7 mg C (mg
Chl)-’ h-l, within the range of marine estimates.
In both freshwater and marine ecosysterns, the percentage algal picoplankton
contribution
to total primary production
tended to increase with depth in the euphotic zone (Costella et al. 1979; Li et al.
1983; Platt et al. 1983a; Craig 1984; Glover
et al. 1985a,b), reflecting, in part, the greater
efficiency of their photopigments to utilize
blue-green light (Li et al. 1983; Wood 1985;
Glover et al. 1985a).
Rates of picoplankton carbon production
showed little variation along eutrophic gradients (Larsson and Hagstrijm
1982) or
among coastal, slope, and open-ocean stations (Glover et al. 19853; Glover 1985),
but the percentage contribution
by picaplankton to total carbon production was
considerably higher in oligotrophic
open
oceans (50-80%) than in meso-eutrophic
coastal marine waters (2-25%) (Stockner and
Antia 1986). A similar trend was also noted
in lakes of varying trophic states (Craig 1984;
Fahnenstiel et al. 1986; Stockner 1987), with
the exception of some episodic midsummer
.
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769
Stockner
770
Table 3. Summary of primary production, biomass, and growth variables for algal picoplankton
and freshwater ecosystems. (Number of investigationsn; see Stockncr and Antis 1986.)
-~
:
Variable
Primary production (mg C m-3 h-l)
(% of total)
Biomass (Chl) (mg m ‘)
(% of total)
Growth AN = mg C (mg Chl)-’ h-l
mg C liter I d- I
I
II= --Ed
mg C liter-l
MARINE
Freshwater
Marine
PELAGIC
Heterotrophic
l-31
(n
l-90
0.5-l-O
(n
l-90
0.3-14.5 (n
0.15-9.0
(n
in marine
= 18)
= 15)
= 8)
= 6)
1-8
(n
16-70
0.3-1.0 (n
0.2-43
2-O-2.7 (n
0.8-1.5 (n
= 5)
= 3)
= 2)
= 1)
cyanobacterial
picoplankton
blooms that
seem to occur in some eutrophic lakes (Bailey-watts et al. 1968; Cronberg and Weibull
198 1). Recently, Joint et al. (1986) reported
the only described seasonal pattern of algal
picoplankton
fluxes in temperate marine
waters, noting that the maximum production rates and relative contribution
to total
phytoplankton production occurred in midsummer (August). Similar seasonal production patterns were observed by Stockncr
(1987) in coastal British Columbia lakes.
Role in aquatic food webs
Chaetognaths
FRESHWATER
Rotifers
PELAGIC
Heterotrophic
Others
Fig. 3. Utilization
of algal picoplankton
in marinc
and freshwater pelagic food webs. Arrow width is subjective estimate of strength of interaction based on the
number of citations in the literature.
It has now been well established that phototrophic picoplankton
can be metabolically a very important part of the pelagic
plankton community, particularly in more
oligotrophic situations where they contribute substantially to total carbon production
and biomass. Like bacteria, the relative constancy oft heir populations during the growing season in temperate
systems, and
thr’oughout the year in tropical and subtropical oceans, implies population control
by predation (Johnson et al. 1982; Campbell 1985; Iturriaga and Mitchell
1986). I
have noted the reported predators of algal
picoplankton in both marine and freshwater
ecosystems in Fig. 3, and have attempted
to depict the degree of interaction by the
width of the arrow.
On the basis of literature reports, heterotrophic flagellates appear to be the principal
predators of algal picoplankton in both marine (Perkins et al. 198 1; Johnson et al. 1982)
and freshwater ecosystems (Boraas et al.
1985; Caron et al. 1985b; Fahnenstiel et al.
1986).
Mixotrophic freshwater flagellates such as
Dinobryon, Ochromonas, and Gymnodini-
771
Phototrophic picoplankton
:.
MlCROLlTERSPHEkE
r-i
CO,
+
NO:
:
+’
CLASS iIC
cnnn
c
PO,LIPHVT~‘GLL~~NI
I
RE’MIN.
L
I
I
-RE
Release
of
DOM
for
f formation
:by photosyn.
iof Ppico
and
:gas
produced
i by epibacteria
and
\ ‘(ferm.
methane)
- - Epibacterial
decay
-
-Sedimentatic
Fig. 4. A model of how numerous components of picoplankton and nanoplankton form three trophic-mode
microcosms in just a few microliters of water to create the basic foundation of life in oligotrophic waters, and
how this understudied part of the food web interfaces with the classic diatom<opepod-fish
food chain. PARPhotosynthetically
active radiation; Cpico-chemolithotrophic
picoplankton;
Ppico-phototrophic
picoplankton; Pnano-phototrophic
nanoplankton;
Hpico-heterotrophic
picoplankton;
Hnano-heterotrophic
nanoplankton; POM-particulate
organic matter; DOM-dissolved
organic matter; DIM-dissolved
inorganic water.
(Reproduced, with permission, from Sieburth and Davis 1982.)
urn are capable of supplementing their photoautotrophic
nutrition
tyith direct ingestion of bacteria and, presumably,
algal
picoplankton
as well (Porter et al. 1985;
Sanders et al. 1985; Bird and Kalff 1986).
Several species of Dinobryon have recently
been shown to have the potential to remove
more bacteria from the water column than
are consumed by crustaceans, rotifers, and
ciliates combined. Algal picoplankton have
already been found in Dinobryon food vac-
uoles (D. Bird pers. comm.), and thus there
is little reason to doubt that they too are an
important component of the diet of these
mixotrophic
flagellates, at least in freshwater.
Ciliates also appear to be significant grazers of algal picoplankton,
but most observations have come from marine waters
(Sherr et al. 1986; Iturriaga and Mitchell
1986). Some freshwater rotifers can utilize
algal picoplankton
(Caron et al. 1985b;
772
Stockner
Stockner 1987), and because of their ubiquity and rapid grazing rates, it is likely that
rotifers may be the major grazer of picoplankton, particularly in oligotrophic lakes.
Chroococcoid cyanobacterial picoplankton have been found in the guts and fecal
pellets of both marine and freshwater copepods, but they appear to be undigested
and viable (Silver and Alldredge
198 1;
Johnson et al. 1982; Caron et al. 19856;
lturriaga and Mitchell 1986). Synechococcus has been observed in the gut of the freshwater cladoceran Eubosmina in coastal
J3ritish Columbia lakes, but appeared undigested (Stockner and Antia 1986).
A host of other metazoan filter feeders in
the marine environment can potentially retain particles l-2 pm in diameter, including
ascidians, bryozoans, pelagic larval stages
of marine invertebrates,
bivalves,
and
sponges. Heaviest grazing by these metazoans would likely occur in estuaries and in
nearshore coastal waters, for it is at these
locations that the greatest abundance and
biomass of picoplankton occur (Johnson and
Sieburth 1982; Gast 1985; Glover 1985).
‘The appendicularian
Oikopleura can effectively filter feed on bacteria (King et al. 1980)
and would likely utilize algal picoplankton
as well, although King et al. do not report
such use. Iturriaga and Mi tchcll (1986) observed considerable numbers of chroococcoid cyanobacteria in the cephalic region of
a chaetognath, suggesting direct utilization
by what is normally considered a primary
carnivore. Further research is necessary to
quantify the significance of algal picoplankton use by a variety of metazoans in lakes
and oceans, but the evidence in hand stronglly suggests population control by predation.
It is important that biological limnologists and oceanographers begin to incorporate phototrophic picoplankton into their
conceptual models of plankton food webs,
especially in the pelagic zone of ultra-oligotrophic systems, where they may be key
components in carbon metabolism and energy transfer, along with their heterotrophic
counterparts - bacteria. One of the best examples of their incorporation
into the food
web of the oligotrophic ocean is provided
by Sieburth and Davis (1982) (Fig. 4). Although conceived as a model of the oligo-
trophic ocean, it can be considered an appropriate representation of the pelagic food
web of large oligotrophic lakes such as the
Laurentian Great Lakes. In fact, the processes depicted in Fig. 4 are germane to most
aquatic systems, irrespective of their trophic condition.
Further research is required to document
molt-e fully the importance of algal picoplankton in waters of varying productivity,
at different latitudes, and at different seasons of the year, as well as the degree to
which they contribute to pelagic food webs,
either as important links in the movement
of carbon to higher trophic levels or as undesirable sinks.
Rejhnces
ALBERTE, R. S., A. M. WOOD, T. A. KURSAR, AND R.
R. L. GIJILLARD. 1984. Novel phycocrythrins
in
marine Synecchococc~s spp. Characterization
and
evolutionary
and ecological implications.
Plant
Physiol. 75: 732-739.
ANDREOLI, C., N. RASCIO, AND G. CASADORO. 1978.
Chlorella ~tana sp. nov. (Chlorophyceae): A new
marine Chlorella. Bot. Mar. 21: 253-256.
ANITA, N. J. 1976. Effects oftemperature on the darkness survival of marine microplanktonic
algae.
Microb. Ecol. 3: 41-54.
-, AND J. Y. CHENG. 1970. The survival of axcnit cultures of marine planktonic algae from prolonged exposure to darkness at 20°C. Phycologia
9: 179-183.
--,
AND -.
1977. Reexamination
of the carotenoid pigments of the unicellular blue-green alga
Agmenellum quadruplicafum. J. Fish. Res. Bd. Can.
34: 659-668.
AZAM, F., AND OTHERS. 1983. The ecological role of
water-column microbes in the sea. Mar. Ecol. Prog.
Ser. 10: 257-263.
BAILEY-WATTS, A. E., M. E. BINDLOSS, AND J. H.
BELCHER. 1968. Freshwater primary production
by a blue-green alga of bacterial size. Nature 220:
1344-l 345.
BANSE, K. 1974. On the role of bacterioplankton
in
the tropical ocean. Mar. Biol. 24: l-5.
BERMAN, T. 1975. Size fractionation ofnatural aquatic populations associated with autotrophic
and
heterotrophic carbon uptake. Mar. Biol. 33: 2 15220.
BIEIVFANG, P. K., AND J. P. SZYPER. 1981. Phytoplankton dynamics in the subtropical Pacific Ocean
otT Hawaii. Deep-Sea Res. 28: 98 I-1000.
BIRD, D. F., AND J. KALFF. 1986. Bacterial grazing
by planktonic lake algae. Science 231: 493-495.
BORAAS, M. E.,C.C. REMSEN,AND D.D. SEALE. 1985.
Phagotrophic flagellate populations in Lake Michigan: Use of image analysis to determine numbers
and size distribution.
Eos 66: 1299.
BRYANT. D.A..G. COHEN-BAZIRE,AND A.N. GLAZER.
Phototrophic picoplankton
198 1.
Characterization
of the biliprotcins
of
content of
a cyanobacterial
phycoerythrin
carrying phycourobilin chromophore. Arch. Microbial.
129: 190198.
BUCHECKER,R.,S. LIAAEN-JENSEN,G.BORCH,ANDH.
W. SIEGELMAN. 1976. Carotenoids of Anacystis
niduluns. Structures of caloxanthin and nostoxanthin. Phytochemistry
15: 10 15- 10 18.
BUTCHER,R. W. 1952. Contributions to our knowledge of the smaller marine algae. J. Mar. Biol.
Assoc. U.K. 31: 175-191.
CAMPBELL,L. 1985. Estimating grazing pressure on
Synechococcusspp. using the seawater dilution and
selective inhibitor techniques for measuring grazing rates. Eos 66: 13 14.
-,
E. J. CARPENTER,AND V. J. IACONO. 1983.
Identification
and enumeration of marine chroococcoid cyanobacteria
by immunofluorescence.
Appl. Environ. Microbial. 46: 553-559.
CARON,D. A.,J.C. GOLDMAN,~. K. ANDERSON,AND
M. R. DENNETT. 1985~. Nutrient cycling in a
microflagellate food chain: 2. Population dynamics and carbon cycling. Mar. Ecol. Prog. Ser. 24:
243-254.
-,
F. R. PICK, ANDD. R. S. LEAN. 1985b. Chroococcoid cyanobacteria in Lake Ontario: Vertical
and seasonal distributions during 1982. J. Phycol.
21: 171-175.
CHANG, V. T.-P. 1980. Zwei neue SynechococcusArten aus dem Zurichsec. Schweiz. Z. Hydrol. 42:
247-254.
CHAPMAN,D. J. 1973. Biliprotcins and bile pigments,
p. 162-185. In N. G. Carr and B. A. Whitton
[eds.], The biology ofblue-green algae. Univ. Calif.
COSTELLA,
A.C.,K.S. SHORTREED,AND
J.G. STOCKNER.
1979. Phytoplankton
fractionation
studies in
Great Central Lake, British Columbia. A nutrientenriched sockeye salmon (Oncorhynchus nerku)
nursery lake. Fish. Mar. Serv. Tech. Rep. 880.
27 p.
CRAIG,S. R. 1984. Productivity of algal picoplankton
in a small meromictic lake. Int. Vcr. Theor. Angew. Limnol. Vcrh. 22: 351-354.
CRONBERG,G.,ANDC.WEIBULL. 198 1. Cyanodictyon
impet-fectum, a new chroococcal blue-green alga
from Lake Trummen, Sweden. Arch. Hydrobiol.
Suppl. 60, p. 101-l 10.
DALEY, R. J. 1979. Direct epifluorescence enumeration of native aquatic bacteria: Uses, limitations,
and comparative accuracy, p. 29-45. In J. W. Costcrton and R. R. Colwell [eds.], Native aquatic
bacteria: Enumeration,
activity,
and ecology.
ASTM STP 695.
DREWS,G., H. PRAUSER,AND D. UHLMANN. 1961.
Massenvorkommen
von Synechococcusplancticus
nov. spec., eincr solit%ren, planktischcn Cyanophyccc, in cinem Abwasserteich.
Beitrag zur
Kenntnis der sogenannten “p-Algen.”
Arch. Mikrobiol. 39: 101-l 15.
EVANS, E. L., AND M. M. ALLEN. 1973. Phycobilisomes in Anacystis nidulans. J. Bact. 113: 403408..
Gloeobacter violaceous. Chromophore
773
FAHNENSTIEL,G. L., L. SICKO-GOAD,D. SCAVIA,AND
E. F. STOERMER.1986. Importance of picoplankton in Lake Superior. Can. J. Fish. Aquat. Sci. 43:
23 5-240.
FOTT, B., AND M. NOVAKOVA. 1969. A monograph
of the genus Chlorella. The freshwater species, p.
10-74. In B. Fott [ed.], Studies in phycology. E.
Schweizerbart’sche.
FRIEBELE,E. S., D. L. CORRELL,AND M. A. FAUST.
1978. Relationship
between phytoplankton
cell
size and the rate of orthophosphate uptake: In situ
observations of an estuarine population. Mar. Biol.
45: 39-52.
GAST, V. 1985. Bacteria as a food source for microzooplankton
in the Schlci Fjord and Baltic Sea
with special reference to ciliates. Mar. Ecol. 22:
107-120.
GEORGE,E. A. 19 57. A note on Stichococcus bacillaris
Naeg. and some species of Chlorella as marine
algae. J. Mar. Biol. Assoc. U.K. 36: 11 l-l 14.
GLOVER,H. E. 1985. The physiology and ecology of
the marine cyanobacterial
genus Synechococcus.
Adv. Aquat. Microbial.
3: 49-107.
-,
M.D. J&LLER,AND R.R.L. GUILLARD. 1986.
Light quality and oceanic ultraphytoplankters.
Nature 319: 142-l 43.
-,
D.A. PHINNEY,ANDC.S.YENTSCH. 1985~.
Photosynthetic
characteristics
of picoplankton
compared with those of larger phytoplankton
populations, in various water masses in the Gulf of
Maine. Biol. Oceanogr. 3: 223-248.
-,
A.E. SMITH,ANDL. SHAPIRO. 1985b. Diurnal
variations in photosynthetic
rates: Comparisons
ofultraphytoplankton
with a larger phytoplankton
size fraction. J. Plankton Rcs. 7: 5 19-535.
GRAY, B.H.,J. COSNER,ANDE. GANTT. 1976. Phycocyanins with absorption maxima at 637 nm and
623 nm from Agmenellum quadruplicatum. Photochcm. Photobiol. 24: 299-302.
GRIITITHS, A. J. 1984. A descriptive numericlature
for isolates of cyanobacteria.
Br. Phycol. J. 19:
233-238.
GUGLIELMI,G.,G.COHEN-BAZIRE,AND D.A. BRYANT.
198 1. The structure of Gloeobacter violaceus and
its phycobilisomes.
Arch. Microbial.
129: 181189.
GUILLARD, R. R. L., L. S. MURPHY, P. Foss, AND S.
LIAAEN-JENSEN. 1985. Synechococcus spp. as
likely zeaxanthin-dominant
ultraphytoplankton
in
the North Atlantic. Limnol. Oceanogr. 30: 412414.
HERTZBERG,S., S. LIAEEN-JENSEN,
AND H. W. SIEGELMAN. 197 1. The carotenoids of blue-green algae.
Phytochemistry
10: 3 12 l-3 127.
HICKEL, B. 198 1. Cyanodictyon rcticulutum (Lemm)
Geitlcr (Cyanophyta), a rare planktonic blue-green
alga refound in eutrophic lakes. Arch. Hydrobiol.
Suppl. 60, p. 11 l-l 18.
HOBBIE,J.E.,R.J. DALEY,ANDS.JASPER. 1977. Use
of Nuclepore filters for counting bacteria by lluorcscence microscopy. Appl. Environ. Microbial.
33: 1225-l 228.
HOLLIGAN,P.M.,R.D.
PINGREE,ANDG.T. MARDELL.
774
Stockner
1985. Oceanic solitons, nutrient pulses and phytoplankton growth. Nature 314: 348-350.
I”TURRIAGA,R., AND B. G. MITC’HELL. 1986. Chroococcoid cyanobacteria: A significant component in
the food web dynamics of the open ocean. Mar.
Ecol. Prog. Ser. 28: 291-297.
JAVORNICKY,P. 1976. Minute species of the genus
Rhodomonas Karsten (Cryptophyceae).
Arch.
Protistenk. 118: 98-106.
JENKINS,W. J., AND J. C. GOLDMAN. 1985. Seasonal
oxygen cycling and primary production in the Sargasso Sea. J. Mar. Res. 43: 465-49 1.
JOHNSON,K. M., C. M. BURNEY, AND J. McN. SIEBURT~I. 198 1. Enigmatic marine ecosystem metabolism measured by direct diel CO, and 0, flux
in conjunction with DOC release and uptake. Mar.
Biol. 65: 49-60.
JOHNSON,P. W., AND J. McN. SIEBURTH. 1979.
Chroococcoid
cyanobacteria in the sea: A ubiquitous and diverse phototrophic biomass. Limnol.
Oceanogr. 24: 928-935.
--,
AND -.
1982. In-situ morphology and
occurrence of eucaryotic phototrophs of bacterial
size in the picoplankton
of estuarine and oceanic
waters. J. Phycol. 18: 3 18-327.
--I
F.-S. Xu, ANI>J. McN. SIEBURTH. 1982. The
utilization of chroococcoid cyanobacteria by marine protozooplankters
but not by Calanoid copepods. Ann. Inst. Oceanogr. Paris 58(suppl.): 297308.
JOINT,I. R., N. J. P. OWENS,AND A. J. POMROY. 1986.
Seasonal production of photosynthetic picoplankton and nanoplankton in the Celtic Sea. Mar. Ecol.
Prog. Ser. 28: 251-258.
-,
AND R. K. PIPE. 1984. An electron microscope study of a natural population of picoplankton from the Celtic Sea. Mar. Ecol. Prog. Ser. 20:
113-118.
KING, K. R., J. T. HOLLIBAUGH,AND F. AZAM. 1980.
Predator-prey
interactions between the larvacean
Oikopleura dioica and bacterioplankton
in enclosed water columns. Mar. Biol. 56: 49-57.
KURSAR,T. A., H. SWIFT, AND R. S. ALBERTE. 198 1.
Morphology of a novel cyanobacterium
and characterization of ligh t-harvesting complexes from it:
Implications for phycobiliprotein
evolution. Proc.
Natl. Acad. Sci. 78: 6888-6892.
L,ANDRY,M. R., L. W. HAAS, AND V. L. FAGERNESS.
1984. Dynamics of microbial plankton communities: Experiments in Kaneohe Bay, Hawaii. Mar.
Ecol. Prog. Ser. 16: 127-133.
LARSSON,U., ANDA. HAGSTR~M. 1982. Fractionated
phytoplankton
primary production,
exudate rclease and bacterial production in a Baltic eutrophication gradient. Mar. Biol. 67: 57-70.
LEHMAN, J. T., AND C. D. SANDGREN. 1982. Phosphorus dynamics of the procaryotic nannoplankton in a Michigan lake. Limnol. Oceanogr. 27:
828-838.
LI, W. K. W., AND OTHERS. 1983. Autotrophic picoplankton in the tropical ocean. Science 219: 292295.
MANTON, I. 1977. Dolichomastix (Prasinophyceae)
from arctic Canada, Alaska and South Africa: A
new genus of flagellates with scaly flagella. Phycologia 16: 427-438.
MOKRIS, I., AND H. GLOVER. 198 1. Physiology of
photosynthesis
by marine coccoid cyanobacteria -some
ecological
implications.
Limnol.
Oceanogr. 26: 957-96 1.
MUNAWAR,M., AND G. L. FAHNENSTIEL. 1982. The
abundance and significance of ultraplankton
and
microalgae at an offshore station in central Lake
Superior. Can. Tech. Rep. Fish. Aquat. Sci. 1153,
p. l-13.
NEILSON,A. H., AND T. LARSSON. 1980. The utilization of organic nitrogen for growth of algae:
Physiological aspects. Physiol. Plant. 48: 542-553.
PAEF~,H. W. 1977. Ultraphytoplankton
biomass and
production in some New Zealand lakes. N.Z. J.
Mar. Freshwater Res. 11: 297-305.
PERKINS,F. O., L. W. HAAS, D. E. PHILLIPS,AND K.
L. WEBB. 198 1. Ultrastructure
of a marine Synechococcus possessing spinae. Can. J. Microbial.
27: 3 18-329.
PLATT, T., D. V. SUBBARAO, AND B. IRWIN. 1983a.
Photosynthesis of picoplankton in the oligotrophic
ocean. Nature 301: 702-704.
-ANDOTHERS.1983b. Photosynthetically
compeient phytoplankton
from the aphotic zone of the
deep ocean. Mar. Ecol. Prog. Ser. 10: 105-l 10.
POMEROY,L. R. 1974. The ocean’s food web, a changing paradigm. Bioscience 24: 499-504.
PORTER, K. G., E. B. SHERR,B. F. SHERR,M. PACE,
AND R. W. SANDERS. 1985. Protozoa in planktonic food webs. J. Protozool. 32: 409-4 15.
PROBYN,T. A. 1985. Nitrogen uptake by size-fractionatcd phytoplankton
populations in the southern Benguela upwelling system. Mar. Ecol. Prog.
Ser. 22: 249-258.
-AND S. J. PAINTING. 1985. Nitrogen uptake
by’size-fractionated
phytoplankton
populations in
Antarctic surface waters. Limnol. Oceanogr. 30:
1327-l 332.
Purr, M., AND B. PREZELIN. 1985. Diurnal patterns
of photosynthesis
in cyanobacteria
and nanoplankton in California coastal waters during “el
Nifio.” J. Plankton Rcs. 7: 779-790.
REYNOLDS,N. 1973. The estimation of the abundance of ultraplankton.
Br. Phycol. J. 8: 135-146.
RIPF’KA,R., J. DERUELLES,
J. B. WATERBURY,M. HERDMAN, ANP>R. Y. STANIER. 1979. Generic assignments, strain histories, and properties of pure cultures of cyanobacteria. J. Gcn. Microbial.
111: l61.
--,
J. WATERBURY,AND G. COHEN-BAZIRE. 1974.
A cyanobacterium
which lacks thylakoids. Arch.
Mikrobiol.
100: 4 19-436.
RODHE,W. 1955. Productivity:
Can plankton production proceed during winter darkness in subarctic lakes? Int. Ver. Theor. Angew. Limnol. Verh.
12: 117-122.
SAXJO,Y. 1964. Size distribution of photosynthesizing phytoplankton
in the Indian Ocean. J. Oceanogr. Sot. Jpn. 19: 187-189.
-, AND K. TAKESUE. 1965. Further studies on
the size distribution
of photosynthesizing
phyto-
Phototrophic picoplankton
plankton in the Indian Ocean. J. Oceanogr. Sot.
Jpn. 20: 264-271.
SANDERS,R. W., K. G. PORTER,AND R. MCDONOUGH.
1985. Bactivory by ciliates, microflagellates
and
mixotrophic
algae: Factors influencing
particle
ingestion. Eos 66: 13 14.
SAROKIN,D. J., AND E. J. CARPENTER. 1982. Ultrastructure and taxonomic observations on marine
isolates of the genus Nannochloris (Chlorophyccac). Bot. Mar. 25: 483-491.
SHERR,E. B., B. F. SHERR,R. D. FALLON, AND S. Y.
NEWELL. 1986. Small, aloricate ciliates as a major component of the marine heterotrophic nanoplankton. Limnol. Oceanogr. 31: 177-183.
SIEBURTH,J. McN., AND P. G. DAVIS. 1982. The role
of heterotrophic nanoplankton in the grazing and
nurturing of planktonic bacteria in the Sargasso
and Caribbean Seas. Ann. Inst. Oceanogr. Paris
58(suppl.): 285-296.
-,
V. SMETACEK,AND J. LENZ. 1978. Pelagic
ecosystem structure: Heterotrophic compartments
of the plankton and their relationship to plankton
size fractions. Limnol. Oceanogr. 23: 1256-1263.
SILVER,M. W., AND A. L. ALLDREDGE. 198 1. Bathypelagic marine snow: Deep-sea algal and detrital
community. J. Mar. Res. 39: 501-530.
SOROKIN,Y. I. 1971. On the role of bacteria in the
productivity
of tropical oceanic waters. Int. Rev.
Gesamten Hydrobiol. 56: l-48.
STOCKNER,J. G. 1987. Lake fertilization:
The enrichment cycle and lake sockeye salmon (Oncorhynchus nerka) production, p. 198-2 15. In Sockeye salmon (Oncorhynchus ncrka) population
biology and future management. Can. Spcc. Publ.
Fish. Aquat. Sci. 96.
AND N. J. ANTIA. 1986. Algal picoplankton
from marine and freshwater ecosystems: A multidisciplinary
perspective. Can. J. Fish. Aquat. Sci.
43: 2472-2503.
STRANSKY,H., ANDA. HAGER. 1970. Das Carotinoidmuster und die Verbreitung dcs lichtinduzierten
Xanthophyllcyclus
in verschiedenen
Algenklassen. 4. Cyanophyccae und Rhodophyceac. Arch.
Mikrobiol.
72: 84-96.
775
SUTTLE,C. A., AND P. J. HARRISON. 1986. Phosphate
uptake rates of phytoplankton
assemblages grown
at different dilution rates in semi-continuous
culture. Can. J. Fish. Aquat. Sci. 43: 1474-148 1.
TAKAHASHI, M., AND P. K. BIENFANG. 1983. Size
structure of phytoplankton
biomass and photosynthesis in subtropical Hawaiian waters. Mar.
Biol. 76: 203-211.
AND T. HORI. 1984. Abundance of picophytoplankton
in the subsurface chlorophyll
maximum layer in subtropical and tropical waters. Mar.
Biol. 79: 177-186.
THRONDSEN,J. 1978. Productivity and abundance of
ultra- and nanoplankton in Osloljordcn. Sarsia 63:
273-284.
TURNER, M. F., AND R. J. GOWEN. 1984. Some aspccts of the nutrition and taxonomy of fourteen
small green and yellow-green algae. Bot. Mar. 27:
249-255.
VOTINTSEV,K. K., A. I. MESHCERYAKOVA,
AND G. I.
POPOVSKAYA. 1972. The importance of ultrananoplanktonic
algae in the primary production
of Lake Baikal in the summer. Gidrobiol. Zh. 8:
2 l-27.
WATERBURY,J. B., S. W. WATSON,R. R. L. GUILLARD,
AND L. E. BRAND. 1979. Widespread occurrence
of a unicellular, marine, planktonic cyanobacterium. Nature 277: 293-294.
WILLIAMS, P. J. LEB. 1984. Bacterial production in
the marine food chain: The emperor’s new suit of
clothes?, p. 271-299. In Flow of energy and materials in marine ecosystems- theory and practice.
NATO Conf. Ser. 4, Mar. Sci. V. 13, Plenum.
WOOD, A. M. 1985. Adaptation of photosynthetic
apparatus of marine ultraphytoplankton
to natural
light fields. Nature 316: 253-255.
-,
AND OTHERS. 1985. Discrimination
between
types of pigments in marine Synechococcus spp.
by scanning spectroscopy,
epifluorescence
microscopy, and flow cytometry. Limnol. Oceanogr.
30: 1303-1315.
WYATT, J. T., AND J. K. G. SILVEY. 1969. Nitrogen
fixation by Gloeocapsa. Scicncc 165: 908-909.