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Interactions of phytoplankton, zooplankton and microorganisms
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P'off
SUMMER
UPWELLING
ON THE
SOUTHEASTERN
CONTINENTAL
SHELF
OF THE U.S.A. DURING 1981
Interactions of Phytoplankton, Zooplankton and Microorganisms L. R. PO",IEROY', G.-A. PAFFE~;H6FER'"
J. A. YODER'"
and
"Department n.t"Zoology & In~glt(ae of Eco[o'~>. Um~ ersttx of Georgta. Adrens. GA 30002. U 5..-t 'Sk~du~a~ Insurute of Oceanogruphy. Sav(mnah. GA 314tJO.-a)667. (..S .4
ABSTRACT We present
evidence t h a t
organisms, d o l i o l i d s stranding
and
there
are s i g n i f i c a n t
Fr~til~aria
on the c o n t i n e n t a l
within
shelf.
During
interactions
intrusions
between h e t e r o t r o p h i c
of n u t r i e n t - r i c h
the summer of
1981 c o l d ,
micro-
Gulf Stream water nutrient-rich
water
from below the surface of the Gulf Stream was r e p e a t e d l y i n t r u d e d and stranded on the continental of
s h e l f o f f n o r t h e a s t e r n F l o r i d a . On August 6 o l d , stranded Gulf Stream water depleted
nitrate
shelf
occupied
water,
older
everywhere at
all
the lower but of
depths,
l a y e r on the outer
undefined age.
shelf.
The upper water was c o n t i n e n t a l
On August 6 f r e e - l i v i n g
an order of magnitude g r e a t e r
b a c t e r i a were >106ml - I
than normal b a c t e r i a l
numbers on
the n o r t h e a s t e r n F l o r i d a c o n t i n e n t a l
s h e l f . Over 10 days the numbers of f r e e b a c t e r i a doubled
w h i l e b a c t e r i a attached to p a r t i c l e s
increased by a f a c t o r of f o u r . The a d e n y l a t e / c h l o r o p h y l l
ratio
showed
surface
that
phytoplankton
water became i n c r e a s i n g l y
protozoa)
over
and d o l i o l i d s
10 days.
in
a highly
locations
stratified
of
Production
Friti~laria
salp swarms.
system in of
layers
of
dominated by h e t e r o t r o p h i c
suggests a d i v e r s e source of b a c t e r i a l as i n t e r m e d i a r i e s .
lower
There were s i g n i f i c a n t ,
and between b a c t e r i a and
did not c o i n c i d e w i t h depths
dominated the
negative
intruded
while
the
microorganisms ( b a c t e r i a
and
correlatiens
are in
distribution,
biomass in much of the surface water and may be s i g n i f i c a n t
the
lower layer
some of which i n v o l v e zooplankton
is more than t w i c e t h a t
of m i c r o h e t e r o t r o p h s
m i c r o h e t e r o t r o p h s are the dominant in energy f l u x
sumers as well as c o m p e t i t o r s f o r m u t u a l l y useable sources of n u t r i t i o n .
353
numbers
The increased numbers of b a c t e r i a at a l l
growth s u b s t r a t e s ,
on average, but because of t h e i r d i f f e r e n t i a l
between b a c t e r i a
Regions of maximum b a c t e r i a l
which most phytoplankton
autotrophs
water,
to metazoan con-
35"
L.R. P~'.IER,_,~ e~".'."
CONTENTS I.
Introduction
354
2.
Methods
355
3.
Observations
356
4.
Discussion
365
5.
Acknowledgements
370
References
370
I. The c o n t i n e n t a l from
s h e l f o f f n o r t h e a s t e r n F l o r i d a is s t r o n g l y i n f l u e n c e d by i n t r u s i o n s of water
subsurface,
nutrient-rich
layers
SHERR, KIRCHMAN and DEIBEL (1983) distribution
INTRODUCTION
of
phytoplankton
of
the
described
as i n d i c a t e d
Gulf the
Stream.
POMEROY, HANSEN, McGILLIVARY,
relationship
by c h l o r o p h y l l
a.
of
bacterial
in the
summer of 1981, a season of unusually intense i n t r u s i o n a c t i v i t y
in t h i s
s e r i e s of r e p o r t s (ATKINSON, LEE, BLANTON and PAFFENHOFER, 1988).
activity
off
northern F l o r i d a
quency and i n t e n s i t y The presence of August
and then o f f of
in
water.
the c o n t i n e n t a l
some phytoplankton
activity
varies
seasonally
over r e l a t i v e l y
long periods
it
of
the
summer wind regime, most i n t r u s i o n s
shelf
regime c o n t r o l l i n g
time during
d e p a r t u r e from the
usual
but the f r e -
and also from year to year. development of move on
over a p e r i o d of a few days, p r o v i d i n g time f o r a bloom but
relatively
little
else.
Upwelling
break is f o r c e d by meandering of the Gulf Stream w i t h a mean p e r i o d i c i t y that
Maximum i n t r u s i o n
Except f o r
and b a c t e r i a ,
a sustained northward wind is
described elsewhere
in summer, when winds from the south p r e v a i l ,
water on the s h e l f
important
shelf
is
intrusion
intruded
1981 was an
communities
of
abundance and
We r e p o r t here observations
necessary to move an i n t r u s i o n
far
at
of 7 days.
the s h e l f However,
enough onto the s h e l f
so
is separated from the west wall of the Gulf Stream as the meander propagates n o r t h -
ward.
Thus,
varies
from year
intrusions
become stranded m a i n l y
to year,
in
depending on the nature
summer, of
and the frequency of
the r e g i o n a l
stranding
wind regime each year
(LEE and PIETRAFESA, 1988). The e x t e n s i v e , stranded i n t r u s i o n s in the summer of 1981 provided an o p p o r t u n i t y
for
the complete u t i l i z a t i o n
more complex communities of organisms. p o p u l a t i o n of the c o n t i n e n t a l Previous
work,
of
intruded
nutrients
and the development of
We d e s c r i b e here the e f f e c t of t h i s on the b a c t e r i a l
s h e l f water.
both on the southeastern c o n t i n e n t a l
shelf
and elsewhere in the ocean, has
shown numbers of b a c t e r i a to be remarkably constant over time and in f a c t to be near 105ml - I in surface waters of the ocean g e n e r a l l y . b a c t e r i a are growing a c t i v e l y
There is also good evidence, however, t h a t these
and indeed t h a t b a c t e r i a l
p r o d u c t i o n is a s i g n i f i c a n t
fraction
Interactlvm~
of
total
355
secondary produc%ion in the ocean (FUHR~AN and AZAM, 1980; AZAM, FENCHEL, FIELD,
GRAY, MEYER-RE!L and THIaGSTAD, 1983; WILLIAMS, 1984). are being consumed
The usual assumption is that b a c t e r i a
by bacteriovores as r a p i d l y as they are produced, and that under most
circumstances the b a c t e r i a are held at or near a "refuge" s i g n i f i c a n t and universal consumers of f r e e - l i v i n g
level
of
abundance.
The most
b a c t e r i a , which make up most of the num-
bers in sea water, are believed to be small f l a g e l l a t e s (FENCHEL, 1984) and c i l i a t e s SHERR, FALLON and NEWELL, 1986). the most l i k e l y
to have some d i r e c t impact on numbers of f r e e - l i v i n g
sea water b a c t e r i a l
bacteria.
numbers usually are l i m i t e d by substrate a v a i l a b i l i t y
than by consumers.
The small
(SHERR,
Among the l a r g e r zooplankton, the pelagic tunicates are
size of f r e e - l i v i n g
any amendment of substrate is evidence of t h a t .
In surface
as much or more
marine b a c t e r i a and t h e i r
response to
In i n t r u s i o n s on the southeastern continental
shelf and in the water adjacent to them we see rapid b a c t e r i a l responses to substrates produced by phytoplankton and possibly by t h e i r consumers.
These are very short-term responses,
appearing in a day and l a s t i n g the two or three days of the usual i n t r u s i o n event (POMEROY, ATKINSON, BLANTON, CAMPBELL, JACOBSEN, KERRICK and WOOD, 1983).
In the summer of 1981 we
had the o p p o r t u n i t y to see what would happen in the longer term, with continuing high rates of production of phytoplankton and the development of populations of consumer zooplankton.
2. Sea water was c o l l e c t e d in cleaned Niskin CTD r o s e t t e . dylate,
samplers attached to e i t h e r
A f t e r s t a i n i n g with a c r i d i n e orange, one or two ml of water was
gently through a O.2um black Sartorius f i l t e r .
We have shown previously t h a t there
is no d i f f e r e n c e in counts on O.2um Sartorius c e l l u l o s e f i l t e r s (Pomeroy
et al.
1983).
The f i l t e r
coverglass sealed with wax. within
a hydro wire or a
Samples were drawn at once, f i x e d in cold glutaraldehyde buffered with caco-
and r e f r i g e r a t e d .
filtered
METHODS
two weeks a f t e r
was mounted in
and O.2um Nuclepore f i l t e r s
low-fluorescence immersion o i l
and the
The s l i d e s were then stored in the dark at +5°C and were counted
the cruise.
A Zeiss standard epifluorescence microscope was used
f o r counting b a c t e r i a at a m a g n i f i c a t i o n of 1250x. Chlorophyll
samples were c o l l e c t e d
on Reeve Angel
984H glass f i b e r
by a m o d i f i c a t i o n of the HPLC method of JACOBSEN (1978).
filters
and measured
Sparging with nitrogen was e l i m i n -
ated from the method, and samples were held in acetone in a f r e e z e r in a l i g h t - p r o o f box. Extraction and HPLC separation were performed a f t e r the cruise. in t h i s paper were always from HPLC. we processed c h l o r o p h y l l and by the method of
Chlorophyll values reported
However, on s t a t i o n s where i t
samples taken from the
YENTSCH and MENZEL (1963).
same Niskin
was possible to db so,
samplers by our HPLC method
The Spearman c o r r e l a t i o n of Jacobsen's
HPLC versus Yentsch and Menzel's f l u o r o m e t r i c method was 0.75 (n:213;
~ =.0001).
The two
c h l o r o p h y l l methods are thus reasonably comparable w i t h i n t h i s data set, although some i n d i v idual
values may d i f f e r
substantially.
However,
the c o r r e l a t i o n of pheophytin a by HPLC
against pheophytin a by the YENTSCH and MENZEL method was 0.33 (a =.0001), i n d i c a t i n g s i g n i f icant differences between the methods in separation of degradation products from each other. In f a c t ,
t h i s may be the p r i n c i p a l source of the d i f f e r e n c e s in the r e s u l t s f o r c h l o r o p h y l l a
356
L R P,I~IERO~~'r Jf
by the two methods.
Primary production was measured with
the 14C method as described
by YODER, ATKINSON, BISHOP, BLANTON, LEE and PIETRAFESA (1935). Adenylate samples were c o l l e c te d on 0.45~m M i l l i p o r e R membrane f i l t e r s into b o i l i n g bicarbonate buffer before reaching t o t a l dryness. with t r i s
buffer and frozen.
which were plunged
The extract was then mixed
Both adenylate and chlorophyll samples were returned to the
laboratory on dry ice and stored at -50°C u n t i l analysis. Zooplankton were collected at the same stations, using a m u l t i p l e opening and closing net. Zooplankton were counted in
50
categories,
to genus and species f o r
some Crustacea and
in broader categories fo r pelagic tunicates, cnidarians, and larval stages of various groups. We converted each of these to biomass, based on the volume of a cylinder with length equal to the median size of the group and a diameter equal to half the length. were t o t a l l e d f o r selected f o r
The 50 categories
each c o l l e c t i o n and in addition categories and sets of categories were
comparison with
numbers of bacteria.
T h e s e were compared by inspection of
the p l o t t e d d i s t r i b u t i o n s and also by c o r r e l a t i o n analysis.
Additional d e t a i l s of the dis-
t r i b u t i o n of zooplankton are in PAFFENHOFER, SHERMANand LEE (1988).
3. On August 6,
OBSERVATIONS
an extensive subsurface intrusion of Gulf Stream water was stranded on the
northeast Fl o r i d a continental
shelf,
running nearly to shore.
The intruded water arrived
on the shelf July 21-30 (LEE and PIETRAFESA, 1988; YODERe;aL]985).
Bottom water temperature
on August 6 was 20°C, and the bottom water had a n i t r a t e anomaly of 4pM. That is, the bottom water n i t r a t e concentration was 4UM less than would be predicted f o r Gulf Stream water at that temperature (ATKINSON, PAFFENHOFERand DUNSTAN, 1978). sion had been in place f o r
This is evidence that the i n t r u -
some time, and phytoplankton had u t i l i z e d much of the o r i g i n a l
nitrate. Current meter data show a d d i t i o n a l cold water intruding on the northeast Flor ida shelf beginning August 6 and continuing u n t i l
August 12 (LEE and PIETRAFESA, 1988).
This August 6-
12 i n t r u s i o n did not penetrate as far toward shore as the previous i n t r u s i o n , so we observed old,
intruded water on the inner continental shelf
and newly intruded water on the outer
shelf.
By August 20 the newly intruded water had moved away or had mixed with older 20°C
water.
During this time the n i t r a t e anomaly became p o s i t i v e on the outer shelf in the region
of newly intruded water but remained negative on the inner shelf. Chlorophyll a was high a l l
across the northeast Florida shelf during August 1981, but i t
was highest in the lower layer near shore, arrived in l a t e July ( F i g . l ) .
in the region occupied by the intrusion that
The influence of the int r us io n of early August can also be
seen in the bottom chlorophyll d i s t r i b u t i o n on August 8-12 near the 40m isobath.
Interactions
s
UPPER ~12
'o . , ~ 31 mo O
,25
35
i
LOWER 8-12
I
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9
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30 N
30N
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.
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t
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UPPER 13-16
.,~~ / .
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J '"
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h
eo w
g
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31N-
LOWER 13-16
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eow
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f
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2 I
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e~
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30 N
30N~
2,
81W •
',
eow
81W
.5 - -
FIG.I.
I J
'.
Chlorophyll a d i s t r i b u t i o n , ug 1- I , on the southeastern c o n t i n e n t a l ~helf of the USA, August 8-12 (top) and 13-16 (bottom) in the upper ( l e f t ) and lower ( r i g h t ) layers of the water column.
80W
,
L. R, PovsRo~ eg al
35x
High rates of primary production were observed during the phytoplankton bloom within intruded waters.
On July 30, peak
rates of primary production were within the thermocline as pre-
viously observed during studies of other intrusions (JACOBSEN, 1981; JACOBSEN, HODSON, MACCUBBIN and POMEROY, 1983), (Fig.2,
YODER e~ a~.
and the d a i l y rate of primary production exceeded 3gC m-ld - l
1985).
Highest rates of Chl a - normalized photosynthesis occurred
within the surface mixed layer. averaged 15.5mgC mg Chl
a-I
Assimilation numbers ( l i g h t - s a t u r a t e d rate of photosynthesis) h- I ,
i n d i c a t i n g that
surface mixed-layer phytoplankton were
growing r a p i d l y (YODERec a~.1985).
20 Aug
% 6 Aug.\ /
A
.-
0
S
,,,,
10
15
20
25
3O
Depth (m) FIG.2.
Depth-time d i s t r i b u t i o n of primary production during and f o l l o w i n g the peak of the phytoplankton bloom within intruded water on the southeastern US continental shelf during the summer, 1981.
F r e e - l i v i n g bacteria were 106ml-I or greater at a l l stations occupied and a l l depths sampled on the continental
shelf
numbers doubled (Fig.3).
during August 1981.
During the two weeks of observation t h e i r
Bacteria attached to p a r t i c l e s ,
which make up about I% of the
t o t a l number of bacteria in the water, are more v a r i a b l e in d i s t r i b u t i o n and abundance than the f r e e - l i v i n g bacteria.
Attached bacteria are most abundant in the regions of the phyto-
plankton blooms associated with on the outer shelf.
the two i n tr u s io n events, one on the inner shelf and one
While f r e e - l i v i n g bacteria doubled during two weeks, loc a liz ed patches
of attached bacteria increased by a f a c t o r of four (Fig.5). The adenylate/chlorophyll r a t i o was used to indicate the dominant biomass in the plankton, exclusive of net zooplankton, in the continental shelf waters (CAMPBELL, JACOBSEN and POMEROY 1979; POMEROYet aL1983).
On August 8-12, phytoplankton dominated the bottom water in both
the early August intrusions and the e n t i r e water column of the late July intrusion (Fig.7). In the upper layer there was a region of heterotrophic dominance (bacteria and protozoa) in mid-shelf, between the two intruded water bodies.
On August 13-16 autotrophic dominance
359
Interactions
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FIG.3.
THERMOCLINE
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' .'
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,, ,0
~
C] UPPER MIXED LAYER
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:
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4
4
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e., f
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LOWER LAYER
Distribution of f r e e - l i v i n g bacteria and of salps on the continental shelf of southeastern USA, August B-16, 1981. [solines show numbers of free bacteria x 106ml-1. Shaded areas show regions where salp numbers were I0m-3 August 13-16, and 25m-3 in the surface water and in the thermocline, and I0m-I in the bottom layer on August 8-12.
'°'
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3~)
L.R. PO~tERO~ ¢:j/
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FIG.4.
i
',
80W
THERMOCLINE
OIW
I 2
4
LOWER LAYER
D i s t r i b u t i o n of f r e e - l i v i n g b a c t e r i a and of d o l i o l i d s on the c o n t i n e n t a l s h e l f of southeastern USA, August 8-16, 1981. I s o l i n e s show numbers of f r e e b a c t e r i a x 106ml - I Shaded areas show regions wh~re d o l i o l i d numbers were >500m-3 August 8-12 and >100m-~August 13-16.
30 N
3t
Interactions
11-12
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FIG.5.
THERMOCLINE
LOWER LAYER
Distribution of bacteria attached co par%i:les and of salps on the continental shelf off the southeastern USA August 8-16, 1981. [soline show numbers of bacteria x 104ml-I Shaded areas show regions where salp numbers were >100m-3 August 13-16; and >25m-3 in the surface water and in the thermocline, and >IOm-3 in the bottom water August 8-12.
;'o°
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.:
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_
of the bottom water diminished on the outer shelf, had become strongly heterotrophic.
while surface water on the outer shelf
At that time the bottom w~ter on the inner shelf remained
dominated by auto;rophs, while the surface showed patches of both autotrophic and heterotrophic dominance.
The greatest microbial
biomass is generaily in the bottom water, but
i t is related to the locations of the intrusions and is dominated by phytoplankton (Fig.8). Comparing the d i s t r i b u t i o n the d i s t r i b u t i o n
of
of free
doliolids
and attached bacteria in
shelf
water
(PAFFENHOFER, SHERMAN and LEE, 1988),
we find
of a reduction in numbers of bacteria where d o l i o l i d s are most abundant. of f r e e - l i v i n g bacteria
bacteria showed l i t t l e
spatial
show a more pronounced r e l a t i o n s h i p ,
the main center of d o l i o l i d s .
(Figs.4,6)
in d ic at ions
Because numbers
v a r i a t i o n during August 8-12, with
with
highest numbers occurring
the attached inshore of
This was a time of peak d o l i o l i d abundance, with maximum
numbers approaching 5,000m-3 in the lower layer of shelf water.
During August 13-16, both
free and attached bacteria show maximum numbers where saIps and d o l i o l i d s are least abundant (Figs 3-6). mum.
At this time d o l i o l i d numbers had declined everywhere from t h e i r previous maxi-
In the lower layer in p a r t i c u l a r ,
of our grid
of observations,
the d o l i o l i d maximum occurred in the southern h a l f
while maxima of f r e e - l i v i n g
in the northern half of the grid.
and attached bacteria occurred
Since the d o l i o l i d data are reported as t o t a l d o l i o l i d s ,
we may not see the r e l a t i o n s h i p with bacteria as c l e a r l y as i f stage of the l i f e doliolids
history were p l o t te d separately.
the d i s t r i b u t i o n
of each
The r e l a t i o n s h i p between bacteria and
is demonstrated by the f o l l o w i n g s t a t i s t i c a l
analysis of bacterial and d o l i o l i d
distributions. To examine possible r e l a t i o n s h i p s
between bacteria and zooplankton, c o r r e l a t i o n analyses
were performed between three groups
of
bacteria and three groups of zooplankton:
total
bacteria, attached bacteria, and f r e e - l i v i n g bacteria versus t o t a l zooplankton, crustaceans, and pelagic tunicates.
C o r r e l a t i o n analyses were performed with counts of
bacteria and
zooplankton, log transformations of the counts, and counts weighted for volume of the zooplankton in each group (Table I ) .
With the volume weighting, tunicates showed a Spearman
c o r r e l a t i o n of -0.40 with t o t a l bacteria (~ : .0001). c o r r e l a t i o n of -0.25 (~ = .002). -0.28
(n=26,
~=0.17).
]ans.
D o ] i o l i d phorozoids showed a Spearman
showed a c o r r e l a t i o n with t o t a l bacteria of
Phorozoids and gonozoids were then combined into a single group,
d o l i o l i d s , while O~kop~ra and
Fritil~aria
and F r i t i ~ l a r i a were combined into a single group, appendicular-
However, c o r r e l a t i o n s of these condensed groups were less negative than f o r phorozoids Frit~Z~ar~a
alone.
untransformed tunicate statistically
A stepwise regression was then performed on both transformed and
components with
free-living
bacteria.
s i g n i f i c a n t components are oozoids, d o l i o l i d s ,
For transformed data, and Oikople~ra
the
(Table 2).
Total zooplankton and crustacean zooplankton are not s i g n i f i c a n t components in these analyses
[rite f a c t i o n s
I '--,,0 ~
uPPER I
8.-12
/
.5 /
.~' I
3IN"
303
s
LOWER
'- - , , o~
8-12
.'v. I
.*"
2 5
I
5
...
,0 ,°~
!
31,N,
i '[
*
,
t #
L /
\
i
/ l:!l
: .5
:'L
/
i
i; 7' / 3 0 N,
30~
\ IIW
L
2
"
(10 W
E3 UPPER MIXED LAYER
FIG.6.
JPO 19:3/4-J
m THERMOCLINE
'
LOWER LAYER
D i s t r i b u t i o n of b a c t e r i a attached to p a r t i c l e s and of d o l i o l i d s on the continental shelf of southeastern USA Augus~ 8-16, 1 9 8 1 . I s o l i n e s show numbers of bacteria x 104ml - I . Shaded areas show regions where d o l i o l i d numbers were >500 m-3 August 8-12 and >lOOm-3 August 13-16.
30a
PO~tERO~ e,~ a /
L.R.
:'-
UPPER
•
w
,,
'
'
.'.~'LOWER
"
=
::~ ::
:~"~~:~:~::%-
'
::::i::'
:
i
i
~
UPPER
"
"
"
,,"
13-15
>
'
'
--, ~
i~iiiii~'-,~
-
.
v-
31 . .
,
30 N-
====================================== ============================== : ,
'.
=
=========================== . 30N
•
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, ~ ;.
,,,
LOWER
"
',
~
'--,,o~
•
oo,.
,"
13-16
*:i~!;
',
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31N-
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~ ~ :
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6 "ii~i~i~. •
,
"::::;
,
:
ili
,
,'
,'
30 N
,
',
~
3 0 N,
i'.
..!.~,.~,, FIG.7.
" ...
.,,~,
..!.-~,,,"
,
.'
..
Distribution of the adenylate/chlorophyll r a t i o on the continental shelf of the southeastern USA, August 816, 1981. Stippled areas are dominated by autotrophs; hatched areas are dominated by heterotrophs; unshaded areas have mixed populations.
:
,o,
lnteracvton~
10
3~5
rs
40ST. AUQUST|NI[
CUMIII[RI.ANO IS.
JACKSONVILLE
ONMOND I t A C H
FIG.8.
ABLE I:
D i s t r i b u t i o n of t o t a l microbial ATP, ~g 1- I on four sections across the continental shelf of southeastern USA during August 1981. Left column: St Augustine section (30°O0'N) on August 6 (top), I0, 14 and 20 (bottom); Cumberland Island section (31°00'N) on August 12 (top) and 16; Ormond Beach section (29°20'N) on August 8 and 13 (bottom); Jacksonville section (30°30'N) on August 7 (top), 11, and 15 (bottom).
Spearman correlation (with a values in parentheses) of natural logarithm transformed data for total bacteria, single, f r e e - l i v i n g bacteria, and bacteria attached to particles, with total zooplankton, crustacean zooplankton, and tunicate zooplankton. N=I70. Samples were taken in continental shelf waters of northeastern Florida August 6 to 22, 1981. Bacteria
Total Zooplankton
CrustaceanZooplankton
Tunicate Zooplankton
Total
-0.161 (0.04)
+0.045 (0.56)
Free
-0.161 (0.04)
+0.039 (0.61)
-0.402 (0.0001) -0.399 (0.0001)
Attached
-0.026 (0.76)
+0.019 (0.81)
-0.236 (0.0035)
5hh
L P,. PO~IERO~.¢tal.
TABLE 2:
Stepwise correlation of f r e e - l i v i n g , single bacteria with groups of zooplankton in the continental shelf waters off Northeastern Florida, August 6-22, 1981. Natural logarithm transformation; p>f = 0.0001 in a l l cases. 1
oozoid
0.4761
2
doliolid
0.7926
3
Oikop~e~ra
0.9789
4
s o l i t a r y salps
0.9967
5
aggregated salps
0.9995
6
phorozoid
1.0000
4.
DISCUSSION
Concurrent c o l l e c t i o n s of data on heterotrophic microorganisms, phytoplankton, and zooplan~on were made to address three questions: ( I)
What are the sources of substrates that support
the predictable increase in b a c t e r i a l numbers and biomass (by at least one order of magnitude) when intrusions significant
are present on the continental shelf?
(2) Do grazing zooplankton have a
impact on the numbers of f r e e - l i v i n g bacteria or those attached to particles?
(3) Are heterotrophic bacteria a s i g n i f i c a n t source of n u t r i t i o n f o r zooplankton, d i r e c t l y or i n d i r e c t l y , or are they competitors f o r resources common to both groups? We do not suggest relationship,
that the c o r r e l a t i o n analysis we have performed proves any
nor
is
it
helpful
in i d e n t i f y i n g specific processes
Indeed, some of the negative results, with chlorophyll ~,
causative
that may be at work.
such as the lack of c o r r e l a t i o n of bacterial numbers
are as i n s t r u c t i v e as the s i g n i f i c a n t c o r r e l a t i o n s .
Having said t h i s ,
we do suggest that this analysis does help us build concepts of food web i n t e r a c t i o n s . I.
It
is
often assumed that the major source of substrates for f r e e - l i v i n g marine
heterotrophic bacteria
is
the
low molecular weight compounds released by phytoplankton.
Thus we might expect a high c o r r e l a t i o n between free bacteria and phytoplankton, or chlorophyll a. is
On the southeastern continental shelf c o r r e l a t i o n of bacteria with chlorophyll
insignificant
(r 2 = +0.09).
Instead,
equally both in the upper layer, in the lower layer, this
the numbers of bacteria increase
where there is a small population of phytoplankton, and
where there is a large population of phytoplankton.
before (POMEROY et a l .
1983),
approximately
We have reported
and have found bacterial numbers elevated in the water
above intrusions on every occasion we have sampled them. Since low molecular weight compounds released by the phytoplankton cannot f r e e l y cross the pycnocline to provide bacterial substrates in the upper layer, the obvious postulate is that v e r t i c a l l y migrating zooplankton are serving as intermediaries in the conversion of phytoplankton to substrates f o r heterotrophic bacteria.
The production of b a c t e r i a l
substrates by zooplankton was demonstrated
experimentally in the Southern C a l i f o r n i a Bight by EPPLEY, HORRIGAN, FUHRMAN, BROOKS, PRICE and SELLNER (1981) and in a microcosm model system by COPPING and LORENZEN (1980). to find
any evidence f o r
this
in the c o r r e l a t i o n analyses of our data f o r
We f a i l e d
the northeast
In[erections
Florida shelf.
However, i f
bacterial
3,~T
substrates from a l l
sources were in excess and did
no~ l i m i t production of bacteria during intrusion events, then we would not detect a p o s i t i v e spatial c o r r e l a t i o n with t o t a l zooplankton, or any of the ~0 components counted separately, even i f
t h e i r c o n t r i b u t i o n were a major one.
The high and s t e a d i l y increasing numbers of
bacteria in surface as well as bottom water suggest that this is the case. 2.
If
bacteria are not s u b s t r a t e - l i m i t e d ,
are they then limited by grazing?
major grazers of bacteria are believed to be protozoa (FENCHEL, 1984; SHERRet a~. Therefore, any impact of metazoan grazers is
The 1986).
superimposed on that of protozoan grazers,
so we should not expect to see a perfect c o r r e l a t i o n of bacterial numbers with zooplankton. In f a c t ,
we f i n d
harvest bacteria,
substantial
partial
the mucus-net
c o r r e l a t i o n s with
feeders (Table I ) .
those zooplankton most l i k e l y
We show s t a t i s t i c a l l y
to
that there is
a s i g n i f i c a n t negative c o r r e l a t i o n between bacteria and the phorozoid and gonozoid stages of Dolio~etta, bacterial
as well as the appendicularian F r i t i L l a r i a .
numbers through nonselective feeding.
the pelagic tunicates,
These have a s i g n i f i c a n t impact on
The d o l i o l i d s are among the smallest of
and they probably have the f i n e s t nets, capable of most e f f i c i e n t l y
removing f r e e - l i v i n g bacteria from the water.
In the CEPEX experiments with enclosed water
columns, KING, HOLLIBAUGH and AZAM (1980) found that the appendicularian, Oikople~ra consumed f r e e - l i v i n g bacteria, but that they did not have s i g n i f i c a n t impact on the size of the bact e r i a l population.
Our observations suggest that Do~io~eCta
is more e f f e c t i v e in removing
bacteria from the water than e i t h e r of the appendicularians Oikop~eura
Do~toletta can have a s i g n i f i c a n t
impact on numbers of
Dol6o~etta gegenbauri in continental
shelf
or F ~ t t i ~ a r i a ,
bacteria in the water.
waters during
August
and
Numbers of
1981 ranged from
zero to
4,700m3, with concentrations of lOOm3 being f a i r l y common. Using feeding rates f o r P.g~2~bo~a~ determined by DEIBEL (1982a), we see that the clearance times f or shelf waters, by D.geg~a~r< alone, w i l l
be about one day at the highest population densities observed and 100 days at
densities around lOOm3, DEIBEL predicted that d o l i o l i d swarms of the highest observed density would have a s i g n i f i c a n t
impact on b a c te r i a l populations, but this
is probably the f i r s t
concurrent data set of d o l i o l i d s and bacteria which make a test of DEIBEL's prediction possible. The negative spatial
r e l a t i o n s h i p between bacteria and d o l i o l i d s
bacteria attached to amorphous organic aggregates, I0-50~m.
is most pronounced for
Probably these r e l a t i v e l y large,
sticky p a r t i c l e s are removed from the water by d o l i o l i d s more e f f i c i e n t l y than single, freeliving
bacteria 0.2pg in diameter.
tunicates themselves.
One source of p a r t i c l e s
Previous studies have shown that
is
the feces of the pelagic
these p a r t i c l e s
have a l i f e t i m e
in the water of 2-3 days i f not consumed by coprophages (POMEROY and DEIBEL, 1980). eraS.(1984) modelled the fate
of d o l i o l i d fecal
themselves might be the p r i n c i p a l consumers.
particles,
POMEROY
suggesting that the d o l i o l i d s
This appears to be supported by the present
observations, which show that organic aggregates, from a l l
sources, with attached bacteria
on them are least abundant where d o l i o l i d s are most abundant.
We see both s t a t i s t i c a l
and
observational evidence that the d o l i o l i d s had an impact on numbers of both free and attached bacteria.
However, the d o l i o l i d s were not c o n s i s t e n t l y abundant enough to drive down the
numbers of f r e e - l i v i n g bacteria below I06mi " I . were r e s t r i c t e d in both time and space (Figs.3-6).
Patches of high d o l i o l i d and salp density
368
L R. PO~IERO~e: ~l.
3. well
If
bacteria are being grazed by mucus-net
feeding zooplankton, and i f
they,
as
as other zooplankton, consume the flagellates and c i l i a t e s that feed principally on
heterotrophio bacteria, should we conclude, as did PACE, GLASSER and POMEROY (1984) that there can be a significant transfer of energy from bacteria to metazoa?
The adenylate/
chlorophyll ratios found in surface water of the continental shelf during our observations in August 1981 suggest that the predominant food for zooplankton much of the time is heterotrophic bacteria and protozoans. Estimates in Table 3 of the range of abundance of the various components of the plankton available to small mucus net feeders show that on average there is 2-I0 times as much autotrophic as micro-heterotrophic biomass and production. However,
biomass is distributed so that there is t y p i c a l l y strong autotrophic dominance of
the lower layer and heterotrophic dominance of the upper layer.
The component groups of
organisms may not be u t i l i z e d in proportion to their abundance or productivity, however. Some of the dominant diatoms are too large for small mucus net feeders to u t i l i z e .
Others,
such as Thalassiosira s u b t i l i s , are small but form large multi-cell aggregates (YODER, ATKINSON, BISHOP, HOFMANNand LEE, 1983). Moreover, observations of the feces of the salp, r h a l i a demooratioa,
allowed to feed in water from Gulf Stream intrusions, showed large numbers
of undigested diatoms and Syneohooooous protozoa (POMEROY and DEIBEL, 1980). microorganisms are assimilated
but v i r t u a l l y no heterotrophic bacteria and no This is circumstantial evidence that heterotrophic
by pelagic tunicates more e f f i c i e n t l y than are the dominant
autotrophs, both prokaryotic and eukaryotic. However, the highest concentrations of doliolids were always found in the lower, autotroph-dominated layer.
Of course, that may have been
a response to factors other than food supply. While the f r e e - l i v i n g bacteria can be eaten only by mucus-net feeders and by microheterotrophs such as protozoans,
the attached bacteria may be eaten by selective-feeding zooplankton
such as copepods (ROMAN, 1984).
MILLS, PITTMAN, and TAN (1984) present evidence from B13C
data that on the Scotian continental shelf copepods are indeed omnivores rather than s t r i c t herbivores. (1985)
This has also been demonstrated experimentally by PAFFENHOFER and VAN SANT
using high-speed cinematopography.
In plankton blooms,
such as those associated
with Gulf Stream intrusions on the southeastern shelf, copepods may be s e l e c t i v e l y ingesting fecal cells.
particles
and other aggregates rich
in microbial
biomass as well
as phytoplankton
Thus, both selective and non-selective feeders may derive s i g n i f i c a n t
energy from attached bacteria. of bacteria,
it
may c o n s t i t u t e POMEROY, 1981).
amounts of
Because they represent only about one per cent of the numbers
is easy to overlook the f a c t that attached bacteria are large in size and a significant fraction
of the b a c t er ial
biomass (cf
HODSON, MACCUBBIN and
During bloom conditions t h e i r rate of production may be as great as that
of f r e e - l i v i n g bacteria.
Bloom conditions favor the production of attached bacteria because
p a r t i c u l a t e substrates as well as dissolved ones are augmented, and during August 1981 we saw a p r o p o r t i o n a t e l y greater increase in numbers of attached bacteria associated with stranded intrusions of Gulf Stream water.
Equally high numbers occurred in bottom water, with
high concentrations of chlorophyll a and in
surface water,
with very low chlorophyll ~.
In both surface and bottom water the highest concentrations of attached bacteria occurred in the same parts of the study area:
in the central
shelf on our most nor t her ly section
o f f Cumberland Island, and along the shelf break through the f u l l regions with stranded intrusions on the bottom.
extent of our study area,
of n o r t h e a s t e r n
5 - 103 - 5 x 105
0.5 5.0
Sgneehooooeus ~
nano & p i c o e u k a r y o t e s +
data, and YODER ( 1 9 8 8 ) .
30 - 250**
0.2 - 2
0 . 5 - 15
0.8 - 4
Production gC 1-1d - I
shelf
w i t h c o m p a r a b l e numbers of
= 50.
at other times,
12 - 50
0 . 0 3 3 - 3.3
0.65-6.5
0 . 5 - 15
and C / c h l o r o p h y l l
i n the same r e g i o n
2 x 103 - 1 x 104
assuming I00 Fg c h l o r o p h y l l / c e l l
* * b a s e d on d a t a of JACOBSEN (1981)
+from c h l o r o p h y l l
*Range based on c o u n t s t a k e n in i n t r u s i o n s bacteria present.
AUTOTROPHS
102 _ 103
5.0
flagellates*
104 - 3 x 105
1.0
attached bacteria
I - 5 x 106
0.25
Biomass gC 1-I
on the c o n t i n e n t a l
0.8 - 4
Stream i n t r u s i o n s
Range of numbers ml - I
in Gulf
HETEROTROPHS free-living bacteria
Mean s i z e m
Florida.
Numbers and biomass of m i c r o o r g a n i s m s
T r o p h i c Group
TABLE 3:
5",/
L R Po,.~R.., :': ,z:'
Our observations of stranded intrusions of Gulf Stream wa:er on the southeastern continental shelf suggest that c y c l i c events drive s h i f t s in :~e foo~ ~eo, producing a constantly changing pattern of energy f l u x .
Those times and places ~ith hig~ Droduction of phytoplankton favor
the development of swarms of mucus-net feeders capable : f
utilizing
food organisms, and at such times there is a d i r e c t t r o p ~ c plankton.
d i r e c t l y the smallest
l i n k of microorganisms to zoo-
However, the e f f i c i e n c y with which the energy :~ microbial biomass is transferred
to zooplankton may be very low (POMEROYe~ c~.198~i. because the phytoplankton run out of n u t r i e n t s ,
These conditions are t r a n s i t o r y , usually
leading zo a crash not only of the phyto-
plankton but of that e n t i r e energy pathway in favor of a more e f f i c i e n t one. slower u t i l i z a t i o n
of more r e f r a c t o r y energy sources
sources w i l l f o l l o w .
Periods of
and dependence on recycled nitrogen
Our observations during the summer of 1981, as well as on some previous
occasions, provide evidence supporting the concept of
a complex marine pelagic food web
that involves not only switching between food sources by species populations, but switching of e n t i r e
pathways with
the accompanying rise
and f a l l
of species populations.
This is
not necessarily a wholly haphazard or random sequence of events, but rather i t is a sequence repeated frequently enough that there are regular p a r t i c i p a n t s in a l l of i t s phases: organisms that take advantage of these frequent changes in order to complete t h e i r l i f e cycles. ples of
the regular p a r t i c i p a n t s
are the pelagic tunicates,
times r e l a t i v e to most of the crustacean zooplankton. times of 3-6 weeks f o r
O ~ege~ba~r~
which have short
Exam-
generation
DEIBEL (1982b) estimated generation
in the Georgia Bight.
His estimate is an order of
magnitude longer than the generation times estimated by HERON (1972),
and one may ask i f
the rates suggested by DEIBEL are s u f f i c i e n t to produce the large concentrations observed. However, DEIBEL's methods are well documented, and the high concentrations may be in part the r e s u l t of physical concentration by c i r c u l a t i o n of the shelf water (RYTHER, 1955; MARGALEF 1956).
ACKNOWLEDGEMENTS
We thank P.A. McGillivary f o r and Shirley Nishino f o r
providing estimates of zooplankton dimensions f or weighting
the s t a t i s t i c a l
This work was supported by contracts
analyses and chlorophyll
and adenylate analyses.
DE-A509-76EVO0639 and DE-A509-76EVO0936 with the US
Department of Energy.
REFERENCES ATKINSON, L.P., T.N. LEE, J.O. BLANTON and G.A. PAFFENHOFER (1988) Summer upwelling on the Southeastern Continental Shelf of the USA during 1981: Hydrographic conditions. Progresa ~n Oceanography, 19, 231-266. ATKINSON, L.P., G.A. PAFFENHOFER and W.M. DUNSTAN (1978) The chemical and b i o l o g i c a l e f f e c t of a Gulf Stream i n t r u s i o n o f f St Augustine, Florida. BuZZet~n o f Marine Scienoe, 28, 667-679. AZAM, F., T. FENCHEL, J.G. FIELD, J.S. GRAY, L.A. MEYER-REiL, and F. THINGSTAD (1983) The ecological r o l e of water column microbes in the sea. ~VarineEcology, Progress Ser~es, 10, 157-263.
lnt~ract~on~
3?I
CAMPBELL, W.B., T.~. JACOBSEN and L.R. POMEROY (1979) Heterotrophic-photoautotrophio index -- a C u a l i t a t i v e oarameter of microbial i n t e r a c t i o n s applied to a Gulf Stream intrusion, Marine 3cience Co,~n.un~cations, 5, 383-398. COPPING, A.E. and C.J. LORENZEN (1980) Carbon budget of a marine phytoplankton-herbivore system with carbon-14 as a tracer. Ltxnologw a ~ Oceanographg, 25, 873-B82. DEI3EL, O (19824) Laboratory measured grazing and the ingestion rates of the salm, rha;~a democratiea Forsk~l, and the d o l i o l i d , Do~o~etta gegenbauri Uljanin iTunicata, Thaliacea). Jou.~.a~ of Plankton Research, 4, 189-201. DEIBEL, D (!982b) Laborator~ determined m o r t a l i t y , fecundity, and growth rates of rhalia democra~ca Forsk~l and Do~toletta gegenba~ri Uljanin (Tunicata, Thaliacea). Journa~ of Plankton Research, 4, 143-153. EPPLEY, R.W., S.G. HORRIGAN, J.A. FUHRMAN, E.R. BROOKS, C.C. PRICE, and K. SELLNER (1981) Origins of dissolved organic matter in southern C a l i f o r n i a coastal waters: experiments on the role of zooplankton. Marine Ecology, Progress Series, 6, 149-159. FENCHEL, T. (1984) Suspended marine bacteria as a food source. In: Plows of E~ergy and Materials in Marine Ecosystems, M.J.R. FASHAM, e d i t o r , Plenum Press, New York, 301-315. FUHRMAN, J.A. and F. AZAM (1980) Bacterioplankton secondary production estimates for coastal waters of B r i t i s h Columbia, Antarctica, and C a l i f o r n i a . Applied and Environmental M~crobiology, 39, 1085-1095. HERON, A.C. (1972) Population ecology of a c o l o n i z i n g species: the pelagic tunicate, r h a l i a democratica, I. Individual growth rate and generation time. Oceologia, 10, 269-293. HODSON, R.E., A.E. MACCUBBIN and L.R. POMEROY (1981) Dissolved adenosine triphosphate u t i l i z a t i o n by f r e e - l i v i n g and attached bacterioplankton. Marine Biology, 65, 43-51. JACOBSEN, T.R. (1978) A q u a n t i t a t i v e method for the separation of chlorophylls a and b from phytoplankton pigments by high pressure l i q u i d chromatography. Marine Science Communications, 4, 33-47. JACOBSEN, T.R. (1981) Autotrophic and heterotrophic actiuity measurements on the continental she~f of the southeastern US. Doctoral d i s s e r t a t i o n , U n i v e r s i t y of Georgia, 196pp. JACOBSEN, T.R., R.E. HODSON, A.E. MACCUBBIN and L.R. POMEROY (1983) Influence of a Gulf Stream i n t r u s i o n on abundance and a c t i v i t y of phytoplankton and bacterioplankton off the coast of Florida, USA. Estuarine Coastal and Shelf Science, 17, 509-520. KING, K.R., J.T. HOLLIBAUGH and F. AZAM (1980) Predator-prey interactions between the l a r vacean Oikopleura dio~ca and bacterioplankton in enclosed water columns. Marine Biology, 56, 49-57. LEE, T.N. and L.J. PIETRAFESA (1988) Summer upwelling on the Southeastern Continental Shelf of the USA During 1981: C i r c u l a t i o n , Progress in Oceanography, 19, 267-312. MARGALEF, R. (1956) Estructura y dinamica de la "purga de mar en la Ria de Vigo. Inuest~gacion Pesquera, 5, 113-134. MILLS, E.L., K. PITTMAN and F.C. TAN (1984) Food-web structure on the Scotian Shelf, Eastern Canada. A study using 14C as a food-chain tracer. Rapports et Proc~s-Verbaux des Reunions, Conseil permanent inteznaational pour l'Exploration de la Mer, 183, 111-118. PACE, M.L., J.E. GLASSER and L.R. POMEROY (1984) A simulation analysis of continental shelf food webs. Marine Biology, 82, 47-63. PAFFENHOFER, G.A. and K.B. VAN SANT (1985) The feeding response of a marine planktonic copepod to quantity and q u a l i t y of p a r t i c l e s . Marine Ecology, Progress Series, 27, 55-55. PAFFENHOFER, G-A., B.K. SHERMAN and T.N. LEE (1988) Summer upwelling on the Southeastern Continental Shelf of the USA during 1981: Abundance, d i s t r i b u t i o n and patch formation of zooplankton. Progress in Oceanography, 19,403-436. POMEROY, L.R. and D. DEIBEL (1980) Aggregation of organic matter by pelagic tunicates. L~mnology and Oceanography, 25, 643-652. POMEROY, L.R., L.P. ATKINSON, J.O. BLANTON, W.B. CAMPBELL, T.R. JACOBSEN, K.H. KERRICK and A.M. WOOD (1983) Microbial d i s t r i b u t i o n and abundance in response to physical and b i o l o g i c a l processes on the continental shelf of southeastern USA. Continenta~ Shelf Research, 2, 1-20. POMEROY, L.R., R.B. HANSON, P.A. McGILLIVARY, B.F. SHERR, D. KIRCHMAN and D. DEIBEL (1984) Microbiology and chemistry of fecal products of pelagic tunicates: rates and fates. Bulletin of Marine Science, 35, 426-439. ROMAN, M.R. (1984) U t i l i z a t i o n of detritus by the copepod,Acartia tonsa. L ~ o l o g y and Oceanography, 29, 949-959.
37Z
L
R.
P:.)~IERo~e: ai
RYTHER, J.H. (1955) Ecology of ~ t o t r o p h i c marine dinoflagella~es with reference to red water conditions. In: T~e ~ i ~ e s c e n ~ of Biological Systems, F.H. JOHNSON, e d i t o r , American Associ~:ion for the Advancement of Science, Washington, 387-414. SHERR, E.8., B.F. SHERR, R.O. FALLON and S.Y. NEWELL (1986) Small a l o r i c a t e c i l i a t e s as a main component of the marine heterotrophic nanoplankton. Limno~ogy ~ Oceanography, 31, 177-183. WILLIAMS, P.J.IeB. (1984) Bacterial production in the marine food chain: The emperor's new s u i t of clothes? In: Flows of Energy and -averva~s ~ . . . . ~n Marine Ecosystems M.J.R. FASHAM, editor, Plenum Press, New York, 271-299. YENTSCH, C.S. and D.W. MENZEL (1963) A method for the determination of phytoplankton chlorophyll and phaeophytin by fluorescence. DeeQ-Sea R e s e a r c h , 10, 221-231. YODER, J.A., L.P. ATKINSON, S.S. ~ISHOP, J.O. BLANTON, T.N. LEE and L.J. PIETRAFESA (1985) Phytoplankton dynamics within Gulf Stream i n t r u s i o n s on the southeastern United States continental shelf. Continental Shegf Research, 4, 611-635. YODER, J.A., L.P. ATKINSON, S.S. BISHOP, E.E. HOFMANN and T.N. LEE (1983) Effect of upwelling on phytoplankton p r o d u c t i v i t y of the outer southeastern United States continental shelf. Continental She;f Research, I, 385-404.
N)-q-~o'; ,;" $0,)0 - 5(; Cee~-lgnl ~ ','~:-;XP~.:gamon Pr=v, plc
P'off
SUMMER
UPWELLING
ON THE
SOUTHEASTERN
CONTINENTAL
SHELF
OF THE U.S.A. DURING 1981
Interactions of Phytoplankton, Zooplankton and Microorganisms L. R. PO",IEROY', G.-A. PAFFE~;H6FER'"
J. A. YODER'"
and
"Department n.t"Zoology & In~glt(ae of Eco[o'~>. Um~ ersttx of Georgta. Adrens. GA 30002. U 5..-t 'Sk~du~a~ Insurute of Oceanogruphy. Sav(mnah. GA 314tJO.-a)667. (..S .4
ABSTRACT We present
evidence t h a t
organisms, d o l i o l i d s stranding
and
there
are s i g n i f i c a n t
Fr~til~aria
on the c o n t i n e n t a l
within
shelf.
During
interactions
intrusions
between h e t e r o t r o p h i c
of n u t r i e n t - r i c h
the summer of
1981 c o l d ,
micro-
Gulf Stream water nutrient-rich
water
from below the surface of the Gulf Stream was r e p e a t e d l y i n t r u d e d and stranded on the continental of
s h e l f o f f n o r t h e a s t e r n F l o r i d a . On August 6 o l d , stranded Gulf Stream water depleted
nitrate
shelf
occupied
water,
older
everywhere at
all
the lower but of
depths,
l a y e r on the outer
undefined age.
shelf.
The upper water was c o n t i n e n t a l
On August 6 f r e e - l i v i n g
an order of magnitude g r e a t e r
b a c t e r i a were >106ml - I
than normal b a c t e r i a l
numbers on
the n o r t h e a s t e r n F l o r i d a c o n t i n e n t a l
s h e l f . Over 10 days the numbers of f r e e b a c t e r i a doubled
w h i l e b a c t e r i a attached to p a r t i c l e s
increased by a f a c t o r of f o u r . The a d e n y l a t e / c h l o r o p h y l l
ratio
showed
surface
that
phytoplankton
water became i n c r e a s i n g l y
protozoa)
over
and d o l i o l i d s
10 days.
in
a highly
locations
stratified
of
Production
Friti~laria
salp swarms.
system in of
layers
of
dominated by h e t e r o t r o p h i c
suggests a d i v e r s e source of b a c t e r i a l as i n t e r m e d i a r i e s .
lower
There were s i g n i f i c a n t ,
and between b a c t e r i a and
did not c o i n c i d e w i t h depths
dominated the
negative
intruded
while
the
microorganisms ( b a c t e r i a
and
correlatiens
are in
distribution,
biomass in much of the surface water and may be s i g n i f i c a n t
the
lower layer
some of which i n v o l v e zooplankton
is more than t w i c e t h a t
of m i c r o h e t e r o t r o p h s
m i c r o h e t e r o t r o p h s are the dominant in energy f l u x
sumers as well as c o m p e t i t o r s f o r m u t u a l l y useable sources of n u t r i t i o n .
353
numbers
The increased numbers of b a c t e r i a at a l l
growth s u b s t r a t e s ,
on average, but because of t h e i r d i f f e r e n t i a l
between b a c t e r i a
Regions of maximum b a c t e r i a l
which most phytoplankton
autotrophs
water,
to metazoan con-
35"
L.R. P~'.IER,_,~ e~".'."
CONTENTS I.
Introduction
354
2.
Methods
355
3.
Observations
356
4.
Discussion
365
5.
Acknowledgements
370
References
370
I. The c o n t i n e n t a l from
s h e l f o f f n o r t h e a s t e r n F l o r i d a is s t r o n g l y i n f l u e n c e d by i n t r u s i o n s of water
subsurface,
nutrient-rich
layers
SHERR, KIRCHMAN and DEIBEL (1983) distribution
INTRODUCTION
of
phytoplankton
of
the
described
as i n d i c a t e d
Gulf the
Stream.
POMEROY, HANSEN, McGILLIVARY,
relationship
by c h l o r o p h y l l
a.
of
bacterial
in the
summer of 1981, a season of unusually intense i n t r u s i o n a c t i v i t y
in t h i s
s e r i e s of r e p o r t s (ATKINSON, LEE, BLANTON and PAFFENHOFER, 1988).
activity
off
northern F l o r i d a
quency and i n t e n s i t y The presence of August
and then o f f of
in
water.
the c o n t i n e n t a l
some phytoplankton
activity
varies
seasonally
over r e l a t i v e l y
long periods
it
of
the
summer wind regime, most i n t r u s i o n s
shelf
regime c o n t r o l l i n g
time during
d e p a r t u r e from the
usual
but the f r e -
and also from year to year. development of move on
over a p e r i o d of a few days, p r o v i d i n g time f o r a bloom but
relatively
little
else.
Upwelling
break is f o r c e d by meandering of the Gulf Stream w i t h a mean p e r i o d i c i t y that
Maximum i n t r u s i o n
Except f o r
and b a c t e r i a ,
a sustained northward wind is
described elsewhere
in summer, when winds from the south p r e v a i l ,
water on the s h e l f
important
shelf
is
intrusion
intruded
1981 was an
communities
of
abundance and
We r e p o r t here observations
necessary to move an i n t r u s i o n
far
at
of 7 days.
the s h e l f However,
enough onto the s h e l f
so
is separated from the west wall of the Gulf Stream as the meander propagates n o r t h -
ward.
Thus,
varies
from year
intrusions
become stranded m a i n l y
to year,
in
depending on the nature
summer, of
and the frequency of
the r e g i o n a l
stranding
wind regime each year
(LEE and PIETRAFESA, 1988). The e x t e n s i v e , stranded i n t r u s i o n s in the summer of 1981 provided an o p p o r t u n i t y
for
the complete u t i l i z a t i o n
more complex communities of organisms. p o p u l a t i o n of the c o n t i n e n t a l Previous
work,
of
intruded
nutrients
and the development of
We d e s c r i b e here the e f f e c t of t h i s on the b a c t e r i a l
s h e l f water.
both on the southeastern c o n t i n e n t a l
shelf
and elsewhere in the ocean, has
shown numbers of b a c t e r i a to be remarkably constant over time and in f a c t to be near 105ml - I in surface waters of the ocean g e n e r a l l y . b a c t e r i a are growing a c t i v e l y
There is also good evidence, however, t h a t these
and indeed t h a t b a c t e r i a l
p r o d u c t i o n is a s i g n i f i c a n t
fraction
Interactlvm~
of
total
355
secondary produc%ion in the ocean (FUHR~AN and AZAM, 1980; AZAM, FENCHEL, FIELD,
GRAY, MEYER-RE!L and THIaGSTAD, 1983; WILLIAMS, 1984). are being consumed
The usual assumption is that b a c t e r i a
by bacteriovores as r a p i d l y as they are produced, and that under most
circumstances the b a c t e r i a are held at or near a "refuge" s i g n i f i c a n t and universal consumers of f r e e - l i v i n g
level
of
abundance.
The most
b a c t e r i a , which make up most of the num-
bers in sea water, are believed to be small f l a g e l l a t e s (FENCHEL, 1984) and c i l i a t e s SHERR, FALLON and NEWELL, 1986). the most l i k e l y
to have some d i r e c t impact on numbers of f r e e - l i v i n g
sea water b a c t e r i a l
bacteria.
numbers usually are l i m i t e d by substrate a v a i l a b i l i t y
than by consumers.
The small
(SHERR,
Among the l a r g e r zooplankton, the pelagic tunicates are
size of f r e e - l i v i n g
any amendment of substrate is evidence of t h a t .
In surface
as much or more
marine b a c t e r i a and t h e i r
response to
In i n t r u s i o n s on the southeastern continental
shelf and in the water adjacent to them we see rapid b a c t e r i a l responses to substrates produced by phytoplankton and possibly by t h e i r consumers.
These are very short-term responses,
appearing in a day and l a s t i n g the two or three days of the usual i n t r u s i o n event (POMEROY, ATKINSON, BLANTON, CAMPBELL, JACOBSEN, KERRICK and WOOD, 1983).
In the summer of 1981 we
had the o p p o r t u n i t y to see what would happen in the longer term, with continuing high rates of production of phytoplankton and the development of populations of consumer zooplankton.
2. Sea water was c o l l e c t e d in cleaned Niskin CTD r o s e t t e . dylate,
samplers attached to e i t h e r
A f t e r s t a i n i n g with a c r i d i n e orange, one or two ml of water was
gently through a O.2um black Sartorius f i l t e r .
We have shown previously t h a t there
is no d i f f e r e n c e in counts on O.2um Sartorius c e l l u l o s e f i l t e r s (Pomeroy
et al.
1983).
The f i l t e r
coverglass sealed with wax. within
a hydro wire or a
Samples were drawn at once, f i x e d in cold glutaraldehyde buffered with caco-
and r e f r i g e r a t e d .
filtered
METHODS
two weeks a f t e r
was mounted in
and O.2um Nuclepore f i l t e r s
low-fluorescence immersion o i l
and the
The s l i d e s were then stored in the dark at +5°C and were counted
the cruise.
A Zeiss standard epifluorescence microscope was used
f o r counting b a c t e r i a at a m a g n i f i c a t i o n of 1250x. Chlorophyll
samples were c o l l e c t e d
on Reeve Angel
984H glass f i b e r
by a m o d i f i c a t i o n of the HPLC method of JACOBSEN (1978).
filters
and measured
Sparging with nitrogen was e l i m i n -
ated from the method, and samples were held in acetone in a f r e e z e r in a l i g h t - p r o o f box. Extraction and HPLC separation were performed a f t e r the cruise. in t h i s paper were always from HPLC. we processed c h l o r o p h y l l and by the method of
Chlorophyll values reported
However, on s t a t i o n s where i t
samples taken from the
YENTSCH and MENZEL (1963).
same Niskin
was possible to db so,
samplers by our HPLC method
The Spearman c o r r e l a t i o n of Jacobsen's
HPLC versus Yentsch and Menzel's f l u o r o m e t r i c method was 0.75 (n:213;
~ =.0001).
The two
c h l o r o p h y l l methods are thus reasonably comparable w i t h i n t h i s data set, although some i n d i v idual
values may d i f f e r
substantially.
However,
the c o r r e l a t i o n of pheophytin a by HPLC
against pheophytin a by the YENTSCH and MENZEL method was 0.33 (a =.0001), i n d i c a t i n g s i g n i f icant differences between the methods in separation of degradation products from each other. In f a c t ,
t h i s may be the p r i n c i p a l source of the d i f f e r e n c e s in the r e s u l t s f o r c h l o r o p h y l l a
356
L R P,I~IERO~~'r Jf
by the two methods.
Primary production was measured with
the 14C method as described
by YODER, ATKINSON, BISHOP, BLANTON, LEE and PIETRAFESA (1935). Adenylate samples were c o l l e c te d on 0.45~m M i l l i p o r e R membrane f i l t e r s into b o i l i n g bicarbonate buffer before reaching t o t a l dryness. with t r i s
buffer and frozen.
which were plunged
The extract was then mixed
Both adenylate and chlorophyll samples were returned to the
laboratory on dry ice and stored at -50°C u n t i l analysis. Zooplankton were collected at the same stations, using a m u l t i p l e opening and closing net. Zooplankton were counted in
50
categories,
to genus and species f o r
some Crustacea and
in broader categories fo r pelagic tunicates, cnidarians, and larval stages of various groups. We converted each of these to biomass, based on the volume of a cylinder with length equal to the median size of the group and a diameter equal to half the length. were t o t a l l e d f o r selected f o r
The 50 categories
each c o l l e c t i o n and in addition categories and sets of categories were
comparison with
numbers of bacteria.
T h e s e were compared by inspection of
the p l o t t e d d i s t r i b u t i o n s and also by c o r r e l a t i o n analysis.
Additional d e t a i l s of the dis-
t r i b u t i o n of zooplankton are in PAFFENHOFER, SHERMANand LEE (1988).
3. On August 6,
OBSERVATIONS
an extensive subsurface intrusion of Gulf Stream water was stranded on the
northeast Fl o r i d a continental
shelf,
running nearly to shore.
The intruded water arrived
on the shelf July 21-30 (LEE and PIETRAFESA, 1988; YODERe;aL]985).
Bottom water temperature
on August 6 was 20°C, and the bottom water had a n i t r a t e anomaly of 4pM. That is, the bottom water n i t r a t e concentration was 4UM less than would be predicted f o r Gulf Stream water at that temperature (ATKINSON, PAFFENHOFERand DUNSTAN, 1978). sion had been in place f o r
This is evidence that the i n t r u -
some time, and phytoplankton had u t i l i z e d much of the o r i g i n a l
nitrate. Current meter data show a d d i t i o n a l cold water intruding on the northeast Flor ida shelf beginning August 6 and continuing u n t i l
August 12 (LEE and PIETRAFESA, 1988).
This August 6-
12 i n t r u s i o n did not penetrate as far toward shore as the previous i n t r u s i o n , so we observed old,
intruded water on the inner continental shelf
and newly intruded water on the outer
shelf.
By August 20 the newly intruded water had moved away or had mixed with older 20°C
water.
During this time the n i t r a t e anomaly became p o s i t i v e on the outer shelf in the region
of newly intruded water but remained negative on the inner shelf. Chlorophyll a was high a l l
across the northeast Florida shelf during August 1981, but i t
was highest in the lower layer near shore, arrived in l a t e July ( F i g . l ) .
in the region occupied by the intrusion that
The influence of the int r us io n of early August can also be
seen in the bottom chlorophyll d i s t r i b u t i o n on August 8-12 near the 40m isobath.
Interactions
s
UPPER ~12
'o . , ~ 31 mo O
,25
35
i
LOWER 8-12
I
,5
i
'~.
o5
9
\ ~\
30 N
30N
II 1I
4
.
°
t
!
.5
UPPER 13-16
.,~~ / .
;
J '"
.25
h
eo w
g
~ °q
31N-
LOWER 13-16
) oo~
| eP
.5
::
eow
'1
f
|
.'~m.
2 I
:~"
•
e~
J
, f
'
30 N
30N~
2,
81W •
',
eow
81W
.5 - -
FIG.I.
I J
'.
Chlorophyll a d i s t r i b u t i o n , ug 1- I , on the southeastern c o n t i n e n t a l ~helf of the USA, August 8-12 (top) and 13-16 (bottom) in the upper ( l e f t ) and lower ( r i g h t ) layers of the water column.
80W
,
L. R, PovsRo~ eg al
35x
High rates of primary production were observed during the phytoplankton bloom within intruded waters.
On July 30, peak
rates of primary production were within the thermocline as pre-
viously observed during studies of other intrusions (JACOBSEN, 1981; JACOBSEN, HODSON, MACCUBBIN and POMEROY, 1983), (Fig.2,
YODER e~ a~.
and the d a i l y rate of primary production exceeded 3gC m-ld - l
1985).
Highest rates of Chl a - normalized photosynthesis occurred
within the surface mixed layer. averaged 15.5mgC mg Chl
a-I
Assimilation numbers ( l i g h t - s a t u r a t e d rate of photosynthesis) h- I ,
i n d i c a t i n g that
surface mixed-layer phytoplankton were
growing r a p i d l y (YODERec a~.1985).
20 Aug
% 6 Aug.\ /
A
.-
0
S
,,,,
10
15
20
25
3O
Depth (m) FIG.2.
Depth-time d i s t r i b u t i o n of primary production during and f o l l o w i n g the peak of the phytoplankton bloom within intruded water on the southeastern US continental shelf during the summer, 1981.
F r e e - l i v i n g bacteria were 106ml-I or greater at a l l stations occupied and a l l depths sampled on the continental
shelf
numbers doubled (Fig.3).
during August 1981.
During the two weeks of observation t h e i r
Bacteria attached to p a r t i c l e s ,
which make up about I% of the
t o t a l number of bacteria in the water, are more v a r i a b l e in d i s t r i b u t i o n and abundance than the f r e e - l i v i n g bacteria.
Attached bacteria are most abundant in the regions of the phyto-
plankton blooms associated with on the outer shelf.
the two i n tr u s io n events, one on the inner shelf and one
While f r e e - l i v i n g bacteria doubled during two weeks, loc a liz ed patches
of attached bacteria increased by a f a c t o r of four (Fig.5). The adenylate/chlorophyll r a t i o was used to indicate the dominant biomass in the plankton, exclusive of net zooplankton, in the continental shelf waters (CAMPBELL, JACOBSEN and POMEROY 1979; POMEROYet aL1983).
On August 8-12, phytoplankton dominated the bottom water in both
the early August intrusions and the e n t i r e water column of the late July intrusion (Fig.7). In the upper layer there was a region of heterotrophic dominance (bacteria and protozoa) in mid-shelf, between the two intruded water bodies.
On August 13-16 autotrophic dominance
359
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FIG.3.
THERMOCLINE
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Distribution of f r e e - l i v i n g bacteria and of salps on the continental shelf of southeastern USA, August B-16, 1981. [solines show numbers of free bacteria x 106ml-1. Shaded areas show regions where salp numbers were I0m-3 August 13-16, and 25m-3 in the surface water and in the thermocline, and I0m-I in the bottom layer on August 8-12.
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FIG.4.
i
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THERMOCLINE
OIW
I 2
4
LOWER LAYER
D i s t r i b u t i o n of f r e e - l i v i n g b a c t e r i a and of d o l i o l i d s on the c o n t i n e n t a l s h e l f of southeastern USA, August 8-16, 1981. I s o l i n e s show numbers of f r e e b a c t e r i a x 106ml - I Shaded areas show regions wh~re d o l i o l i d numbers were >500m-3 August 8-12 and >100m-~August 13-16.
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FIG.5.
THERMOCLINE
LOWER LAYER
Distribution of bacteria attached co par%i:les and of salps on the continental shelf off the southeastern USA August 8-16, 1981. [soline show numbers of bacteria x 104ml-I Shaded areas show regions where salp numbers were >100m-3 August 13-16; and >25m-3 in the surface water and in the thermocline, and >IOm-3 in the bottom water August 8-12.
;'o°
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"
":.~°"
.',.,:
.:
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_
of the bottom water diminished on the outer shelf, had become strongly heterotrophic.
while surface water on the outer shelf
At that time the bottom w~ter on the inner shelf remained
dominated by auto;rophs, while the surface showed patches of both autotrophic and heterotrophic dominance.
The greatest microbial
biomass is generaily in the bottom water, but
i t is related to the locations of the intrusions and is dominated by phytoplankton (Fig.8). Comparing the d i s t r i b u t i o n the d i s t r i b u t i o n
of
of free
doliolids
and attached bacteria in
shelf
water
(PAFFENHOFER, SHERMAN and LEE, 1988),
we find
of a reduction in numbers of bacteria where d o l i o l i d s are most abundant. of f r e e - l i v i n g bacteria
bacteria showed l i t t l e
spatial
show a more pronounced r e l a t i o n s h i p ,
the main center of d o l i o l i d s .
(Figs.4,6)
in d ic at ions
Because numbers
v a r i a t i o n during August 8-12, with
with
highest numbers occurring
the attached inshore of
This was a time of peak d o l i o l i d abundance, with maximum
numbers approaching 5,000m-3 in the lower layer of shelf water.
During August 13-16, both
free and attached bacteria show maximum numbers where saIps and d o l i o l i d s are least abundant (Figs 3-6). mum.
At this time d o l i o l i d numbers had declined everywhere from t h e i r previous maxi-
In the lower layer in p a r t i c u l a r ,
of our grid
of observations,
the d o l i o l i d maximum occurred in the southern h a l f
while maxima of f r e e - l i v i n g
in the northern half of the grid.
and attached bacteria occurred
Since the d o l i o l i d data are reported as t o t a l d o l i o l i d s ,
we may not see the r e l a t i o n s h i p with bacteria as c l e a r l y as i f stage of the l i f e doliolids
history were p l o t te d separately.
the d i s t r i b u t i o n
of each
The r e l a t i o n s h i p between bacteria and
is demonstrated by the f o l l o w i n g s t a t i s t i c a l
analysis of bacterial and d o l i o l i d
distributions. To examine possible r e l a t i o n s h i p s
between bacteria and zooplankton, c o r r e l a t i o n analyses
were performed between three groups
of
bacteria and three groups of zooplankton:
total
bacteria, attached bacteria, and f r e e - l i v i n g bacteria versus t o t a l zooplankton, crustaceans, and pelagic tunicates.
C o r r e l a t i o n analyses were performed with counts of
bacteria and
zooplankton, log transformations of the counts, and counts weighted for volume of the zooplankton in each group (Table I ) .
With the volume weighting, tunicates showed a Spearman
c o r r e l a t i o n of -0.40 with t o t a l bacteria (~ : .0001). c o r r e l a t i o n of -0.25 (~ = .002). -0.28
(n=26,
~=0.17).
]ans.
D o ] i o l i d phorozoids showed a Spearman
showed a c o r r e l a t i o n with t o t a l bacteria of
Phorozoids and gonozoids were then combined into a single group,
d o l i o l i d s , while O~kop~ra and
Fritil~aria
and F r i t i ~ l a r i a were combined into a single group, appendicular-
However, c o r r e l a t i o n s of these condensed groups were less negative than f o r phorozoids Frit~Z~ar~a
alone.
untransformed tunicate statistically
A stepwise regression was then performed on both transformed and
components with
free-living
bacteria.
s i g n i f i c a n t components are oozoids, d o l i o l i d s ,
For transformed data, and Oikople~ra
the
(Table 2).
Total zooplankton and crustacean zooplankton are not s i g n i f i c a n t components in these analyses
[rite f a c t i o n s
I '--,,0 ~
uPPER I
8.-12
/
.5 /
.~' I
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303
s
LOWER
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8-12
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E3 UPPER MIXED LAYER
FIG.6.
JPO 19:3/4-J
m THERMOCLINE
'
LOWER LAYER
D i s t r i b u t i o n of b a c t e r i a attached to p a r t i c l e s and of d o l i o l i d s on the continental shelf of southeastern USA Augus~ 8-16, 1 9 8 1 . I s o l i n e s show numbers of bacteria x 104ml - I . Shaded areas show regions where d o l i o l i d numbers were >500 m-3 August 8-12 and >lOOm-3 August 13-16.
30a
PO~tERO~ e,~ a /
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:'-
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,
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i'.
..!.~,.~,, FIG.7.
" ...
.,,~,
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,
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..
Distribution of the adenylate/chlorophyll r a t i o on the continental shelf of the southeastern USA, August 816, 1981. Stippled areas are dominated by autotrophs; hatched areas are dominated by heterotrophs; unshaded areas have mixed populations.
:
,o,
lnteracvton~
10
3~5
rs
40ST. AUQUST|NI[
CUMIII[RI.ANO IS.
JACKSONVILLE
ONMOND I t A C H
FIG.8.
ABLE I:
D i s t r i b u t i o n of t o t a l microbial ATP, ~g 1- I on four sections across the continental shelf of southeastern USA during August 1981. Left column: St Augustine section (30°O0'N) on August 6 (top), I0, 14 and 20 (bottom); Cumberland Island section (31°00'N) on August 12 (top) and 16; Ormond Beach section (29°20'N) on August 8 and 13 (bottom); Jacksonville section (30°30'N) on August 7 (top), 11, and 15 (bottom).
Spearman correlation (with a values in parentheses) of natural logarithm transformed data for total bacteria, single, f r e e - l i v i n g bacteria, and bacteria attached to particles, with total zooplankton, crustacean zooplankton, and tunicate zooplankton. N=I70. Samples were taken in continental shelf waters of northeastern Florida August 6 to 22, 1981. Bacteria
Total Zooplankton
CrustaceanZooplankton
Tunicate Zooplankton
Total
-0.161 (0.04)
+0.045 (0.56)
Free
-0.161 (0.04)
+0.039 (0.61)
-0.402 (0.0001) -0.399 (0.0001)
Attached
-0.026 (0.76)
+0.019 (0.81)
-0.236 (0.0035)
5hh
L P,. PO~IERO~.¢tal.
TABLE 2:
Stepwise correlation of f r e e - l i v i n g , single bacteria with groups of zooplankton in the continental shelf waters off Northeastern Florida, August 6-22, 1981. Natural logarithm transformation; p>f = 0.0001 in a l l cases. 1
oozoid
0.4761
2
doliolid
0.7926
3
Oikop~e~ra
0.9789
4
s o l i t a r y salps
0.9967
5
aggregated salps
0.9995
6
phorozoid
1.0000
4.
DISCUSSION
Concurrent c o l l e c t i o n s of data on heterotrophic microorganisms, phytoplankton, and zooplan~on were made to address three questions: ( I)
What are the sources of substrates that support
the predictable increase in b a c t e r i a l numbers and biomass (by at least one order of magnitude) when intrusions significant
are present on the continental shelf?
(2) Do grazing zooplankton have a
impact on the numbers of f r e e - l i v i n g bacteria or those attached to particles?
(3) Are heterotrophic bacteria a s i g n i f i c a n t source of n u t r i t i o n f o r zooplankton, d i r e c t l y or i n d i r e c t l y , or are they competitors f o r resources common to both groups? We do not suggest relationship,
that the c o r r e l a t i o n analysis we have performed proves any
nor
is
it
helpful
in i d e n t i f y i n g specific processes
Indeed, some of the negative results, with chlorophyll ~,
causative
that may be at work.
such as the lack of c o r r e l a t i o n of bacterial numbers
are as i n s t r u c t i v e as the s i g n i f i c a n t c o r r e l a t i o n s .
Having said t h i s ,
we do suggest that this analysis does help us build concepts of food web i n t e r a c t i o n s . I.
It
is
often assumed that the major source of substrates for f r e e - l i v i n g marine
heterotrophic bacteria
is
the
low molecular weight compounds released by phytoplankton.
Thus we might expect a high c o r r e l a t i o n between free bacteria and phytoplankton, or chlorophyll a. is
On the southeastern continental shelf c o r r e l a t i o n of bacteria with chlorophyll
insignificant
(r 2 = +0.09).
Instead,
equally both in the upper layer, in the lower layer, this
the numbers of bacteria increase
where there is a small population of phytoplankton, and
where there is a large population of phytoplankton.
before (POMEROY et a l .
1983),
approximately
We have reported
and have found bacterial numbers elevated in the water
above intrusions on every occasion we have sampled them. Since low molecular weight compounds released by the phytoplankton cannot f r e e l y cross the pycnocline to provide bacterial substrates in the upper layer, the obvious postulate is that v e r t i c a l l y migrating zooplankton are serving as intermediaries in the conversion of phytoplankton to substrates f o r heterotrophic bacteria.
The production of b a c t e r i a l
substrates by zooplankton was demonstrated
experimentally in the Southern C a l i f o r n i a Bight by EPPLEY, HORRIGAN, FUHRMAN, BROOKS, PRICE and SELLNER (1981) and in a microcosm model system by COPPING and LORENZEN (1980). to find
any evidence f o r
this
in the c o r r e l a t i o n analyses of our data f o r
We f a i l e d
the northeast
In[erections
Florida shelf.
However, i f
bacterial
3,~T
substrates from a l l
sources were in excess and did
no~ l i m i t production of bacteria during intrusion events, then we would not detect a p o s i t i v e spatial c o r r e l a t i o n with t o t a l zooplankton, or any of the ~0 components counted separately, even i f
t h e i r c o n t r i b u t i o n were a major one.
The high and s t e a d i l y increasing numbers of
bacteria in surface as well as bottom water suggest that this is the case. 2.
If
bacteria are not s u b s t r a t e - l i m i t e d ,
are they then limited by grazing?
major grazers of bacteria are believed to be protozoa (FENCHEL, 1984; SHERRet a~. Therefore, any impact of metazoan grazers is
The 1986).
superimposed on that of protozoan grazers,
so we should not expect to see a perfect c o r r e l a t i o n of bacterial numbers with zooplankton. In f a c t ,
we f i n d
harvest bacteria,
substantial
partial
the mucus-net
c o r r e l a t i o n s with
feeders (Table I ) .
those zooplankton most l i k e l y
We show s t a t i s t i c a l l y
to
that there is
a s i g n i f i c a n t negative c o r r e l a t i o n between bacteria and the phorozoid and gonozoid stages of Dolio~etta, bacterial
as well as the appendicularian F r i t i L l a r i a .
numbers through nonselective feeding.
the pelagic tunicates,
These have a s i g n i f i c a n t impact on
The d o l i o l i d s are among the smallest of
and they probably have the f i n e s t nets, capable of most e f f i c i e n t l y
removing f r e e - l i v i n g bacteria from the water.
In the CEPEX experiments with enclosed water
columns, KING, HOLLIBAUGH and AZAM (1980) found that the appendicularian, Oikople~ra consumed f r e e - l i v i n g bacteria, but that they did not have s i g n i f i c a n t impact on the size of the bact e r i a l population.
Our observations suggest that Do~io~eCta
is more e f f e c t i v e in removing
bacteria from the water than e i t h e r of the appendicularians Oikop~eura
Do~toletta can have a s i g n i f i c a n t
impact on numbers of
Dol6o~etta gegenbauri in continental
shelf
or F ~ t t i ~ a r i a ,
bacteria in the water.
waters during
August
and
Numbers of
1981 ranged from
zero to
4,700m3, with concentrations of lOOm3 being f a i r l y common. Using feeding rates f o r P.g~2~bo~a~ determined by DEIBEL (1982a), we see that the clearance times f or shelf waters, by D.geg~a~r< alone, w i l l
be about one day at the highest population densities observed and 100 days at
densities around lOOm3, DEIBEL predicted that d o l i o l i d swarms of the highest observed density would have a s i g n i f i c a n t
impact on b a c te r i a l populations, but this
is probably the f i r s t
concurrent data set of d o l i o l i d s and bacteria which make a test of DEIBEL's prediction possible. The negative spatial
r e l a t i o n s h i p between bacteria and d o l i o l i d s
bacteria attached to amorphous organic aggregates, I0-50~m.
is most pronounced for
Probably these r e l a t i v e l y large,
sticky p a r t i c l e s are removed from the water by d o l i o l i d s more e f f i c i e n t l y than single, freeliving
bacteria 0.2pg in diameter.
tunicates themselves.
One source of p a r t i c l e s
Previous studies have shown that
is
the feces of the pelagic
these p a r t i c l e s
have a l i f e t i m e
in the water of 2-3 days i f not consumed by coprophages (POMEROY and DEIBEL, 1980). eraS.(1984) modelled the fate
of d o l i o l i d fecal
themselves might be the p r i n c i p a l consumers.
particles,
POMEROY
suggesting that the d o l i o l i d s
This appears to be supported by the present
observations, which show that organic aggregates, from a l l
sources, with attached bacteria
on them are least abundant where d o l i o l i d s are most abundant.
We see both s t a t i s t i c a l
and
observational evidence that the d o l i o l i d s had an impact on numbers of both free and attached bacteria.
However, the d o l i o l i d s were not c o n s i s t e n t l y abundant enough to drive down the
numbers of f r e e - l i v i n g bacteria below I06mi " I . were r e s t r i c t e d in both time and space (Figs.3-6).
Patches of high d o l i o l i d and salp density
368
L R. PO~IERO~e: ~l.
3. well
If
bacteria are being grazed by mucus-net
feeding zooplankton, and i f
they,
as
as other zooplankton, consume the flagellates and c i l i a t e s that feed principally on
heterotrophio bacteria, should we conclude, as did PACE, GLASSER and POMEROY (1984) that there can be a significant transfer of energy from bacteria to metazoa?
The adenylate/
chlorophyll ratios found in surface water of the continental shelf during our observations in August 1981 suggest that the predominant food for zooplankton much of the time is heterotrophic bacteria and protozoans. Estimates in Table 3 of the range of abundance of the various components of the plankton available to small mucus net feeders show that on average there is 2-I0 times as much autotrophic as micro-heterotrophic biomass and production. However,
biomass is distributed so that there is t y p i c a l l y strong autotrophic dominance of
the lower layer and heterotrophic dominance of the upper layer.
The component groups of
organisms may not be u t i l i z e d in proportion to their abundance or productivity, however. Some of the dominant diatoms are too large for small mucus net feeders to u t i l i z e .
Others,
such as Thalassiosira s u b t i l i s , are small but form large multi-cell aggregates (YODER, ATKINSON, BISHOP, HOFMANNand LEE, 1983). Moreover, observations of the feces of the salp, r h a l i a demooratioa,
allowed to feed in water from Gulf Stream intrusions, showed large numbers
of undigested diatoms and Syneohooooous protozoa (POMEROY and DEIBEL, 1980). microorganisms are assimilated
but v i r t u a l l y no heterotrophic bacteria and no This is circumstantial evidence that heterotrophic
by pelagic tunicates more e f f i c i e n t l y than are the dominant
autotrophs, both prokaryotic and eukaryotic. However, the highest concentrations of doliolids were always found in the lower, autotroph-dominated layer.
Of course, that may have been
a response to factors other than food supply. While the f r e e - l i v i n g bacteria can be eaten only by mucus-net feeders and by microheterotrophs such as protozoans,
the attached bacteria may be eaten by selective-feeding zooplankton
such as copepods (ROMAN, 1984).
MILLS, PITTMAN, and TAN (1984) present evidence from B13C
data that on the Scotian continental shelf copepods are indeed omnivores rather than s t r i c t herbivores. (1985)
This has also been demonstrated experimentally by PAFFENHOFER and VAN SANT
using high-speed cinematopography.
In plankton blooms,
such as those associated
with Gulf Stream intrusions on the southeastern shelf, copepods may be s e l e c t i v e l y ingesting fecal cells.
particles
and other aggregates rich
in microbial
biomass as well
as phytoplankton
Thus, both selective and non-selective feeders may derive s i g n i f i c a n t
energy from attached bacteria. of bacteria,
it
may c o n s t i t u t e POMEROY, 1981).
amounts of
Because they represent only about one per cent of the numbers
is easy to overlook the f a c t that attached bacteria are large in size and a significant fraction
of the b a c t er ial
biomass (cf
HODSON, MACCUBBIN and
During bloom conditions t h e i r rate of production may be as great as that
of f r e e - l i v i n g bacteria.
Bloom conditions favor the production of attached bacteria because
p a r t i c u l a t e substrates as well as dissolved ones are augmented, and during August 1981 we saw a p r o p o r t i o n a t e l y greater increase in numbers of attached bacteria associated with stranded intrusions of Gulf Stream water.
Equally high numbers occurred in bottom water, with
high concentrations of chlorophyll a and in
surface water,
with very low chlorophyll ~.
In both surface and bottom water the highest concentrations of attached bacteria occurred in the same parts of the study area:
in the central
shelf on our most nor t her ly section
o f f Cumberland Island, and along the shelf break through the f u l l regions with stranded intrusions on the bottom.
extent of our study area,
of n o r t h e a s t e r n
5 - 103 - 5 x 105
0.5 5.0
Sgneehooooeus ~
nano & p i c o e u k a r y o t e s +
data, and YODER ( 1 9 8 8 ) .
30 - 250**
0.2 - 2
0 . 5 - 15
0.8 - 4
Production gC 1-1d - I
shelf
w i t h c o m p a r a b l e numbers of
= 50.
at other times,
12 - 50
0 . 0 3 3 - 3.3
0.65-6.5
0 . 5 - 15
and C / c h l o r o p h y l l
i n the same r e g i o n
2 x 103 - 1 x 104
assuming I00 Fg c h l o r o p h y l l / c e l l
* * b a s e d on d a t a of JACOBSEN (1981)
+from c h l o r o p h y l l
*Range based on c o u n t s t a k e n in i n t r u s i o n s bacteria present.
AUTOTROPHS
102 _ 103
5.0
flagellates*
104 - 3 x 105
1.0
attached bacteria
I - 5 x 106
0.25
Biomass gC 1-I
on the c o n t i n e n t a l
0.8 - 4
Stream i n t r u s i o n s
Range of numbers ml - I
in Gulf
HETEROTROPHS free-living bacteria
Mean s i z e m
Florida.
Numbers and biomass of m i c r o o r g a n i s m s
T r o p h i c Group
TABLE 3:
5",/
L R Po,.~R.., :': ,z:'
Our observations of stranded intrusions of Gulf Stream wa:er on the southeastern continental shelf suggest that c y c l i c events drive s h i f t s in :~e foo~ ~eo, producing a constantly changing pattern of energy f l u x .
Those times and places ~ith hig~ Droduction of phytoplankton favor
the development of swarms of mucus-net feeders capable : f
utilizing
food organisms, and at such times there is a d i r e c t t r o p ~ c plankton.
d i r e c t l y the smallest
l i n k of microorganisms to zoo-
However, the e f f i c i e n c y with which the energy :~ microbial biomass is transferred
to zooplankton may be very low (POMEROYe~ c~.198~i. because the phytoplankton run out of n u t r i e n t s ,
These conditions are t r a n s i t o r y , usually
leading zo a crash not only of the phyto-
plankton but of that e n t i r e energy pathway in favor of a more e f f i c i e n t one. slower u t i l i z a t i o n
of more r e f r a c t o r y energy sources
sources w i l l f o l l o w .
Periods of
and dependence on recycled nitrogen
Our observations during the summer of 1981, as well as on some previous
occasions, provide evidence supporting the concept of
a complex marine pelagic food web
that involves not only switching between food sources by species populations, but switching of e n t i r e
pathways with
the accompanying rise
and f a l l
of species populations.
This is
not necessarily a wholly haphazard or random sequence of events, but rather i t is a sequence repeated frequently enough that there are regular p a r t i c i p a n t s in a l l of i t s phases: organisms that take advantage of these frequent changes in order to complete t h e i r l i f e cycles. ples of
the regular p a r t i c i p a n t s
are the pelagic tunicates,
times r e l a t i v e to most of the crustacean zooplankton. times of 3-6 weeks f o r
O ~ege~ba~r~
which have short
Exam-
generation
DEIBEL (1982b) estimated generation
in the Georgia Bight.
His estimate is an order of
magnitude longer than the generation times estimated by HERON (1972),
and one may ask i f
the rates suggested by DEIBEL are s u f f i c i e n t to produce the large concentrations observed. However, DEIBEL's methods are well documented, and the high concentrations may be in part the r e s u l t of physical concentration by c i r c u l a t i o n of the shelf water (RYTHER, 1955; MARGALEF 1956).
ACKNOWLEDGEMENTS
We thank P.A. McGillivary f o r and Shirley Nishino f o r
providing estimates of zooplankton dimensions f or weighting
the s t a t i s t i c a l
This work was supported by contracts
analyses and chlorophyll
and adenylate analyses.
DE-A509-76EVO0639 and DE-A509-76EVO0936 with the US
Department of Energy.
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