LIMNOLOGY
March 1976
AND
Volume 21
Number
OCEANOGRAPHY
of phytoplankton
Limitation
Edward
Woods
2
species in the ocean off western Africa1
M. Hulbuti
Hole
Oceanographic
Institution,
Woods
Hole,
Massachusetts
02543
Abstract
The growth rate of phytoplankton
off the west coast of Africa appeared not to be nutrient limited for two reasons. First, most of the species characteristic
of nonupwelling
regions did not show increased abundance in upwelling
or productive
regions where nuSecond, in an upwelling
region, where diatoms
trient or other species were abundant.
dominated,
nutrients
exceeded the half-saturation
values characteristic
of diatoms.
A deductive model of the nutrient
cycle, covering a complete range of nutrient concentrations, is used to interpret the field data. Since most species in the nonupwelling
region were not limited, i.e. were not prevented from being abundant, by the small excess
of nitrogen there, the compound statement ‘cells in the nonupwelling
region were prevented from being abundant and cells in the upwelling
region were not prevented
from
of cells and excess
being abundant’ is false. Instead, the statement that ‘co-occurrence
nitrogen, with small and large amounts in the respective regions, was harmonious’
is true.
Nutrient cycling in the near-surface water of the ocean is eligible as an instance of
symmetry. What is meant by symmetry is
shown by the following sentences. ‘If nutrient gained by phytoplankton cells limited
the number of cells produced-then-lost
to
grazing and sinking ( N ), then the cells
thus lost, after excretion and decomposition
to assimilable nutrient, limited the amount
of nutrient gained ( G ) ‘. Where ‘if’ and
‘then’ clauses are connected by the symbol
3 and key letters in parentheses represent
the two clauses, the quoted sentence can
be written symbolically:
N 1 G.
(1)
But, statement 1 in reverse could conceivably be just as true, for ‘if cells lost limited
’ Contribution
No, 3535 from the Woods Hole
This study was supOceanographic
Institution.
ported by Atomic Energy Commission
contracts
AT (30-l)-3862
(NYO-3862-17)
and AT (ll-l)3564 ( COO-3564-S > and National Science Foundation grant GA-29300.
LIMNOLOGY
AND
OCEANOGRAPHY
nutrient gained ( G), then nutrient gained
limited cells produced-then-lost
(N)‘, or
G 1 N.
(2)
cycling ap-
Both ways of reporting nutrient
pear equally appropriate.
The difficulty with a symmetrical model
of cycling is that it makes the concept of
limitation
an empty locution.
For when
it is said that ‘if nutrient gained limited. , .,
then. . .‘, the claim is that limitation due
to nutrient is necessary to the succeeding
limitation-but
not the reverse. For the
concept of limitation to be meaningful, the
first mentioned limitation must be necessary to the sequence that follows, and that
sequence must be contingent on the first
limitation, following the format for causation presented by Ducasse ( 1969, p. 56).
This claim is the criterion for asymmetry
(Bunge 1959, p. 39,244; Copi 1973, p. 130).
Rather than leaving it merely the reverse
of 1, a source for the sequences of limitation can be inserted in statement 2. Thus
193
MARCH
1976,
V.
21( 2)
Hulburt
CAPE
VERDE
ISL
MONROVIA
‘_,
-,-T=,
Fig. 1. The coast of western Africa,
Verde Islands, and the Canary Islands.
the Cape
a third sentence can bc formulated as follows. ‘If cells produced-then-lost
limited
nutrient gained ( G), then if total nutrient
available was at a very low, growth-ratelimiting concentration ( C ) , then the nutrient gained limited cells produced-then-lost
(N)‘:
G>
GIN).
(3)
Epplcy et al. (1973) present a well documented case for presence of nutrient limitation in the eastern North Pacific Ocean and
statements 1 and 3 appear to bc appropriate
for the conditions observed there. But
later it will be shown that this model can be
transformed to one of symmetry, C 1 [(N
1 G) - (G 1 N)],, where the center dot
means ‘and’, Thus a rate-limiting
nutrient
concentration entails a symmetrical nutrient
cycle, in which gain and loss equal each
other but in which the limitation of gain
by loss is annulled by the limitation of loss
by gain.
Suppose that nutrients were not at a very
low,
growth-rate-limiting
concentration.
This possibility will be considered in describing the plankton and nutrient distributions along the western coast of Africa (Fig,
1). It will be shown that the species resident in nonupwelling regions were not limitcd in their growth rate by nutrient concentration and that those in an upwelling
region were not limited to any marked degrcc by nutrient.
In the tropical waters off western Africa
light could not bc limiting, at least near
the surface. There is then the possibility
that the amount of zooplankton limited the
amount of phytoplankton.
In the nonupwellmg region, where’ phytoplankton
concentration
was low, grazers may have
prevented large concentrations of phytoplankton from occurring. But this would
seem to violate the criterion of asymmetry.
For the claim that grazers limit phytoplankton-i.e.
prevent large amounts from occurring- is refuted by the claim that the
small amount of phytoplankton
limits the
amount of zooplankton-i.e.
prevents large
amounts of zooplankton from occurring.
By possessing an inherently low rate of
growth, resident cells in the nonupwelling
region may limit the production of cells
that are subsequently lost. Such a limitation
will be found to be the outcome of an ecological context-a
context in which the occurrencc of cells does not prevent the occurrence of nutrient,
i.e. in which the
co-occurrence of these entities is harmonious. Though this will be shown to bc the
case for nonupwelling
regions, limitation
will he found not to apply to both nonupwelling and upwelling regions. Thus only
the statement that the co-occurrence of cntities is harmonious applies to both regions.
But to clear the way for the acceptance of
this simple conclusion, a subtle mixture of
facts and logical structure is necessary.
I am indebted to J. T. Lehman for his
able review of this article. The complex
deduction 1 is due to him. I am grateful
to R. W. Doyle, I. R. Copi, and P. B. Ort-
Phytoplankton
linkiation
GYMNODINIUM
PUNCTATUM
GEPHYROCAPSA
OCEAN ICA
CELLS PER
Fig. 2. The surface distribution
ber-13 November
1970.
of abundant
ner for reading the manuscript, to J. H.
Ryther and N. Corwin for nutrient and oxygen data, and K. 0. Emery for collecting
some of the samples. E. W. Conybear
drafted the figures.
Methods
Surface samples for phytoplankton
cnumcration were taken by Van Dorn sampler
and widcsprcad
species off northwest
Africa,
3 Octo-
or by bucket and examined alive or after
preservation
with
formaldehyde.
Most
samples were counted in the living condition; this was preferable since small naked
flagellates were more easily seen when
alive. Lugol’s preservative, which preserves
flagellates fairly well, could not be used,
because it destroys coccolithophorid
species; therefore plankton had to be concen-
196
Ilulburt
.
NlTlSCHlA
L-. DELICATISSIMA
r)
. .
.,
0.
\
.
ib
I EPTOCYLINDRUS
I,_ DfiNlCUS
“1
.
GEPHYROCAPSA,,
8
’
”
i
RHIZOSOLENIA
CaPE
VERDE
IS
GYMNODINIUM
‘,/
”
,)
‘IO
.
1 -
.
(@
10 - 100
100 - 1000
IO
IJMBELLOSPHAEFi’A
IRREGULARIS
II
Fig. 3. The surface distribution
of abundant
and widespread species off central Africa, 22 February-1 May 1973.
trated by centrifugation rather than by settling. Six 17-cm3 tubes were filled with
sample, centrifuged, and, after the supernatant was sucked off, filled with more
sample and again centrifuged.
After rcmoval of the supernatant again, the remaining fluid from all tubes (about 1 cm3 each)
was transferred to a single tube; this was
filled with sample, centrifuged,
and the
residual fluid transferred to a slide under
a rectangular cover slip for counting. Some
cells may have been lost during transfer
from the six tubes to one tube and from
thcrc to the’ slide, but this would be a systematic error and could not vitiate the rcgional comparisons to be presented. More
small naked flagellates were
important,
counted using this method and at a number
of stations they were the dominant species.
Finally, one species, Gymnodinium
punctatum (a naked flagellate),
was only occasional at stations on a cruise where
samples were’ preserved
but occurred
everywhere on the same cruise where they
were counte’d alive
The distribution
of
this species was thercforc shown only for
that half of the cruise where live samples
were counted (see Fie;. 3).
Where species were less abundant than
1 cell cm-3, 33-50 cm3 of sample was
starched, giving a concentration for 1 cell
count&d of 0.03-0.02 cells cmd3. Where
species were as abundant as 100 ceI1.scrnw3
or more, as little as 3.3 cm3 of sample was
starched.
The 25 species shown in Figs. 2-4 were
the most abundant or most widcspre’ad of
the more than 100 species counted. All
species over 10 cells cm-3 in at least one
sample were included in Figs. 24. Figure
2 shows all species that occurred at more
than 45% OFthe stations; Fig, 3 includes all
species that occurred at more than 60% of
the stations.
The nomenclature
of the 25 species
shown in Figs. 24 was that oE Cupp ( 1943)
for diatoms, and that of Gaarder and Hasle
( 1971) and Borsctti and Cati ( 1972) for
coccolithophores
(except for Coccolithus
huxleyi, this being the synonym in Gaarder
and Hasle and Emiliania huxleyi the synonym in Borsetti and C,ati) . GymnrocZinium
punctatum is described in Pouchet ( 1887)
and Martin ( 1929), and Katodinium rotundatum in Campbell ( 1973). The appearance of this last species in ocean water differcd somewhat from its appearance in
estuarine water. In the ocean it always
has a delicate pelliclc, in estuaries it usually does not; in the ocean it is wide with
short hypoconc, in estuaries it is usually
more elongate and thus has a longer hypoCOllC.
Nitrate
and nitrite were determined by
the methods of Wood et al. (1967) and
Strickland and Parsons ( 1965). Since nitrite values were usually less than 0.1 PI;atom liter-l they were added to the nitrate
Phytoplankton
iimitation
THALASSIOSIRA
DECI PI ENS
I -a
ASTERIONELLA
CHAETOCEROS
DEClPl(NS
ci
I.
\
L;EP;X&;LINDRUS
THALASSIONEMA
NITZCHIOIDES
NITZSCHIA
RH I ZOSOLEN IA
STOLTERFOTHI I DELICATISSIMA
*.
o.
0.
0
NITZCHIA
CHAETOCEROS
THALASSIOSIRA
SUBTILIS
X
\
X
0
Fig, 4.
< 1.0
The surface
l
1 - 10
distribution
IO - 100
0 100 - 1000
CELLS PER CM3
l
of abundant
spccics off southwest
Africa,
@ 4000
23 April-11
May
1968.
198
Hulburt
1. Rules of inference.
Table
1. Modus Pollens
(M.P.)
If
Pa(1
P / .*. q
2. Modus Tollens
Syllogism
P"q
q
q;
(I: thereEore
not p
(D.S.)
P or 4;
not p: therefore
"PI.'*
9
4. Simplification
Logical
p
5. Conjunction
p and q: therefore
p
(Conj.)
P
p
6. Addition
l
(1
P;
q: therefore
p and q
p: therefore
p or q
(Add.)
13 / .**
p v q
7. De Morgan's
Theorems
Q(P * q) 3 (q
(De M.)
v Qq)
'L(P v q> = (%P qq)
8. Commutation
(Corn.)
l
(P
4) = ((1 * p)
l
(p " 4) = ((1 " P>
9. Tautology
(Taut.)
P f
(P v P>
10. Double
Negation
(D.N.)
p:wJp
11.
Tr'ansposition
(Trans.)
(PSI) G(",4 3QP)
12. Material
Implication
(PA)
13. Material
:
(Impl.)
(%P v 4)
Equivalence
procedure
q
(Simp.)
p ' q / .*.
4 / .-•
p, then
not
sp
3. Disjunctive
q;
(M.T.)
If
Pdl
*q / .-.
p, then
p: therefore
mind when considering the absolute values
shown in Fig. 5. But for the purposes of
this investigation it was considered best to
include the ammonia data in order to indicate merely that an appreciable amount was
present. All that is required for the arguments presented is that some ammonia
should be present; the absolute concentration is never a relevant issue.
(Equiv.)
(P 3, (1) 3 r(Pd'(q3pl]
values. Ammonia, silicate, and oxygen
wcrc determined by the methods of Solorzano (1969), Grasshoff (1964), and Thompson and Robinson ( 1939).
In conversation with J. J. McCarthy and
E. J. Carpenter K have been impressed by
the possibility of overestimate of the concentrations of arnmonia off northwest Africa. Greater concentrations can be obtained when samples have been frozen and
stored and then analyzed (as done here)
than when samples are analyzed directly
after collecting, This should be borne in
The data obtained by these methods are
prcsentcd. Next the data are organized and
knitted together by the methods of symbolic logic. Sentences arc formulated as in
the introduction
and the clauses of these
sentences are connected by four key words,
‘if’, ‘then’, ‘or’, ‘and’. The ‘if-then’ structure
was illustrated in the introduction.
The
connectives ‘or’, represented by V, ‘and
reprcscnted by ., also join clauses into
complete sentence structure. The clauses
of sentences may be rearranged and recombined according to 19 rules of inference
given by Copi ( 1973). The rules used in
this study arc given in Table 1, where p
and Q represent clauses, where / .‘. means
‘thcrcfore’, where - means ‘not’ or ‘it is not
the case that. , .‘, and where’ = means ‘is
equivalent to. . .‘.
Rules 7, 11, and 12 are the important
principles of De Morgan’s theorems, transposition, and material implication
respectively. These are explained fully in the
section on evidence for absence of nutrient
limitation.
In later sections a number of
deductions are presented.
Each has a
formal structure, consisting of hypotheses,
the first of which are separated and which
constitute the framework of each logical
model. The statements following these hypotheses are logical expressions that can
bc derived from the hypotheses by the rules
of deductive reasoning just described. Tentative hypotheses erected in the course of
the reasoning are displaced to the right of
the initial hypotheses and are separated
from them by vertical lines (see deduction
II ) . Steps of a proof that are not hypotheses
are steps of reasoning, each derived from
the step or steps indicated at its right and
Phytoplankton
one of the rules of inference. The vertical
lines provide a convenient means of keeping track of these temporary hypotheses,
for delimiting any reasoning contingent on
them, and for showing the points in the
deductive argument at which they cease
to operate. For example, a hypothesis may
be connected by 1 to any logical conclusion
contingent on it (Le. to any statement along
the same vertical line as the hypothesis),
and the combined statemeint is moved to
the left of that vertical line, a process known
as conditional proof (Cl?.), and shown in
statement 8 of deduction 1. Indirect proof,
shown in steps lo-18 of deduction 1, is another means of using tentative hypotheses
to reach a conclusion. At the start of an
indirect proof, one assumes the opposite of
what one wishes to prove. When in the
course of reasoning a contradiction emerges
(for example, N a “N), the hypothesis dcnied is connected by 3 to the conclusion,
the hypothesis undenied. By means of a.
series of conditional proofs and indirect arguments, a final conclusion can bc reached
which is subject only to the original hypotheses of the logical model (deduction 1,
line 40). This method of deductive reasoning thus helps one to discover the implications of a whole series of hypotheses, particularly when those implications are not
apparent by less formal means.
The use of ‘if’ is varied, ‘If resident cells
limited cells produced-then-lost’,
as in dcduction 2, is a way of indicating what is
necessary before the cells produced-then10st could limit the amount of nutrient regenerated. ‘If cells were predominantly
round in form’, as in deduction 4, is a way
of stating an option between two actually
occurring sets of objects, round cells and
not-round cells. ‘If cells occurred, then
excess ammonia occurred’, as in deductions
6 and 7, is an emphatic way of saying that
two kinds of things occurred together in a
sample of water from a given location, that
if you got one, you would predictably get
the other. But there is an important innuendo to ‘if’ in ‘if cells occurred’; the intent
of ‘if’ is to rule out the conceivable but not
actual option ‘cells did not occur’.
199
limitation
NORTHWEST
AFRICA
SOUTHWEST
AFRICA
NO,
t
Q
zoo- I’
0
;,2i
. -.I,.
*
*
.
* /
,,;--30
*
,, -.!, ,.!-!
,,,I
.,;,5-!L
! .-!--I-: ,A,
:
3’
.::,< ---::\\t,:
. I -I5
,,’ “Q.P-. ‘\\
10, ‘, .\ :‘:.
Y..
.
,-:’
. . \
--- ____ ,.’
‘+Jj’
,$$. \ . ‘,y
x
/
‘\
.
“.z---;
____ .----*----.,&;4
\. ,,-:
,’ .,1&J (2,) .
I
.
.
*,..
/’ 3b
I’ *
1
-.
100
---.\,,,
,
,.,,4
Si
0,
Fig. 5. The distribution
of nutrients and oxygen off northwest
Africa and southwest
Africa.
Values for nutrients are in ,ug-atoms liter” and for
oxygen in ml liter-‘.
Evidence for absence of nutrient
limitation
Off northwest Africa most observations
were made in water beyond the effect of
upwelling.
But in the southern part of the
survey area were four stations adjoining the
seaward margin of an area of upwelling
(Cincco-Charcot
11, NO Jean Churcot
1971). In a section north of this arca (Fig.
5)) nitrate was negligible in the near-surface
layer ( between 40 and 60 m deep) and incrcascd with depth; ammonia occurred in
appreciable amounts, about 1 pug-atom N
liter-I, in the near-surface layer as well as
deeper. Surface distributions
of species,
200
Hulburt
shown in Fig,. 2, were of three kinds, One
was typified by the coccolithophore
Urnhellosphaera tends, occurring repeatedly
throughout the survey area but always at
low
concentrations. A second was typified
by C. huxleyi and Gephyrocapsa oceanica,
widespread and more abundant off the upwelling area than elsewhcrc. The third
kind was typified by the diatom Nitzschia
seriatn, very abundant just off the upwelling
area but absent or occasional evcrywhcre
else.
Consider a pair of species selected from
the U. ten&s group, a group composed of
five coccolithophorid and two dinoflagellate
species . Umbellosphaera ten& and K. rotundatum had overlapping distributions in
much-but
not all-of
the area surveyed.
They did not have the potentiality to grow
under beneficial nutrient
conditions because they did not occur in abundance ‘as
did N. seriata. Thus ‘nutrient concentration did not limit the growth rate of one
species of the pair when singZy occurring
(-S) and it did not limit them when co-occurring (-CO)‘.
Briefly put this statement
is
-s * -co.
(4
Any pair of species selected from this group
would be eligible to fulfill statement 4.
At the four southern stations adjoining
the upwelling region it is unlikely that any
of the species from the U. ten&s group
could have been abundant. This is supported by short .term (3-5 days) cnrichn-rent experiments of natural populations
( Hulburt and Corwin 19,69), which consistently showed that these species would
not respond to added nutrient, whereas C.
lauxleyi and a variety of diatoms did respond
and grew rapidly.
Although
C. huxleyi was widespread
throughout the area surveyed and capable
of responding to added nutrient, it is impossible to infer that it was not nutrient
limited where its abundance was high but
was nutrient limited where its abundance
was low. Consider the following statements.
‘If C. huxleyi was abundant, as at the southern margin of the area ( B ), then nutrient
did not limit C. f~~xkyi (-CU)‘:
B 1 -CH.
(5)
By the principles of transposition (Trans.)
and double negation (D.N.) (see Table 1)
6 is obtained:
CH 1 “B;
(6)
‘if nutrient did limit C. huxleyi ( CH), then
C. huxleyi was not abundant, as in the major
part of the area (“B)‘.
In 5 we infer that
nutrient did not limit C. huxleyi. But in 6
the inference of nutrient limitation is impossible; instead, nutrient limitation is assumed in order that we may infer that C.
huxleyi was not abundant.
Suppose that
the arguments of 5 and 6 were reversed as
follows: if nutrient did not limit C. huxleyi,
then C. huxleyi was abundant; if C. huxkyi
was not abundant, then nutrient did limit it.
Here, in the second if-then sequence the
inference of nutrient limitation is achieved
-but only by assuming absence of nutrient
limitation
in the first if-then sequence.
What we would wish is to infer absence
and presence of nutrient limitation in both
5 and 6 ( or in their reversed forms). But
this is impossible when the logical procedures are adhered to.
Indirect evidence of absence of nitrogen
limitation in tropical water is afforded by
the observation of Morris et al. ( 1971)
that dark uptake of CO2 was not increased
by ammonia added when natural populations were first brought into the laboratory
-uptake was only so increased after a day
or two when some member or members of
the natural population grew. Presumably,
such a member could not belong to the U.
ten&s type of species, and if such a membcr were C. huxleyi, what has been just
said of C. huxleyi would apply. ( Further
discussion is found in the resume.)
Returning to the evidence of species distributions to support the position of absencc of nutrient limitation, thcrc are presented in Fig. 3 three widespread species,
K. rotundaturn, Discosphaera tubifer, and
Umbellosphaera irregularis.
Two of these
were also in the U. tenuis group of Fig. 2.
These three spccics occurred repeatedly
over the vast area surveyed, but tended to
bc less frequent in the northern part near
the Cape Verde Islands. This failure of
Phytoplankton
occurrence was due in part to the smaller
volume of sample c’xamined because a number of species were so very abundant. The
abundant species occurred not only close
to the coast but also far away from the
coast among the Cape Verde Islands and
southward. The’y were diatoms, except for
a single flagellate (a 3-6-p sphere). Coccolithus huxleyi and G. oceanica were, as
in Fig. 2, widcsprcad; these two were more
abundant in the northern region, along
with the diatoms and the flagellate. Distinctivc of this region was a mixture of the
three kinds of species ( corroborating Hentschel’s 1936 observations); the three widespread species did not respond to the bcncficial northern conditions and were thus, I
suggest, not nutrient limited.
A region of upwelling was observed off
southwest Africa. Figure 5 shows how high
nitrate and silicate concentrations reached
the surface in the southern, near-shore twothirds of the arca surveyed. Though there
was some nutrient
stratification
in the
southern part, stratification
was marked
only in the northern, nonupwelling
part of
the arca. Oxygen, however, was intensely
stratified cvcrywhcre along the length of
the survey area.
Figure 4 shows the surface distributions
of many abundant diatom species; a prcdominance and diversity of diatoms was
also found by Hart and Currie (1960).
Only two nondiatoms occurred, C. huxleyi
and G. oceanica. At one location there was
a great abundance and excessive dominance
of Cliaetoceros socic&s. At three locations
close together the abundance of cells was
split between Chaetoceros &cipiens
and
Chaetoceros didymus. For these and the
other species in the southern, near-shore
two-thirds of the area there was no marked
shortage of nitrate or silicate. These nutricnts should not have limited growth rates
markedly, since the half -maximum uptake
rates for a number of diatoms ‘arc 0.5-5.5
and 0.8-3.4 lug-atoms N and Si liter-l (Eppley et al. 1969; Paasche 1973) and the
amounts in the surface water were 5-20
and 2-20 pg-atoms N and Si liter-l. Therefore ‘either nutrient concentration did not
limitation
201
markedly limit the growth of the singly occurring C. sociaZis ( -S ) or it did not markcdly limit the growth of the co-occurring C.
cZecipiens and C. diclymus (-CO)‘,
whcrc
‘markedly’ means at or below the concentration range of the half-maximum uptake
rate :
-s v -co.
(7)
Here, there are two quite independent
cases, because no common species linked
them together. Either one case by itself or
the other by itself, and certainly both togcther, would be enough to deny the position that nutrient concentration markedly
limited the growth of all three species,
-(S
- CO),
(8)
a statement derived from 7 b,y De Morgan’s
thcorcm. In addition, Fig. 4 shows in the
southern, near-short portion many instances
of spccics pairs, with a single occurrence of
one species of the pair at one station and
co-occurrence of both at another stationso the statcmcnt -S . -CO applies.
In the following section a complex logical model of nutrient cycling will bc prcsentcd. But it will bc found that the model,
so satisfactory for the facts of the nonupwelling region, will be unsatisfactory for
those of the upwelling
region. Then, in
succeeding sections, the pursuit of #alogical
model applicable to both regions will bc
carried, I bclievc, to a successful concluI
sion.
Limitation
in an asymnwtric
nutrient
cycle
The model of the nutrient cycle prcsentcd in the introduction--N
3 G; G 2
( C 1 N)-can
now be extended. Limitation of production either b’y nutrient concentration or b,y resident producer cells is
considered possible. The second possibility
would bc operative in cast nutrient concentration was not low enough to limit growth
rate. These possibilities are expressed as
the first three hypotheses in deduction 1.
The deduction arrives ,at an expression of
the nutrient cycle, by rearranging the following four clauses :
N = ‘nutrient
gained limited
the number
Hulburt
202
of cells produced-then-lost
to grazing and
sinking’;
T = ‘number of resident cells limited the
number of cells produced-then-lost
to grazing and sinking’;
G = ‘cells lost limited nutrient gained’;
C = ‘nutrient
concentration
was 10,~
enough to limit growth rate’.
Step 40 is a brief presentation
of
{C’[(N’G)
- (G’WII
- (4 1 [(T 2 G) - (G 2 T)]},
which reads ‘if nutrient concentration was
low enough to limit growth rate ( C), then
if nutrient gained limited cells producedthen-lost (N) then cells lost limited nutrient
gainecl ( G), and if cells lost limited nutrient
gained (G) then nutrient gained limited
cells produced-then-lost
(N) and likewise if
nutrient concentration was not low enough
to limit growth rate (WC), then if resident
cells limited. . .‘.
Step 40 is thus a full statement covering
limitation at all naturally occurring nutrient
concentrations.
Step 40 can be applied to
the observations off northwest Africa (deduction 2). Step 5 of this deduction is a
brief form of (T EJG) . (G 1 T). This is
an asymmetric model of nutrient cycling:
‘if resident cells limited cells producedthen-lost to grazing and sinking, then cells
lost limited nutrient gained; and if lost cells
limited nutrient gainecl, then. . .‘. There is
a break in the statement after the second
‘then’, for the claim is not the strong claim
asscrtcd by the expression ‘first sequence of
limitation being necessary to the second’,
as cxemplificd by the first if-and-then sequence before the semicolon, The claim
put forward is a weak, contextual claim.
If lost cells did in. fact limit nutrient gained
-that is, if production limited regeneration
-then, in such a context other sequences
of limitation did in fact occur, as, for example, the limitation of the production of
these lost cells b.y the number of resident,
producer cells. In this way the nutrient
cycle is properly reported for observations
off northwest (Fig. 2) and probably off
central Africa ( Fig. 3)) where the hypothe-
Deduction
1
1.
:NvT)~G
HYP.
2.
:a(C=‘N)
HYP.
3.
zB(N-!3
1I
fIYP*
4.
5.
G
HYP.
6.
C=rN
HYP.
F
N
7.
:SN
8.
2,
5,
6,
4,
M.P.
M.P.
5-7,
9.
C.P.
IIYP.
11.
IIYP.
1, Trans.
12.
11,
10, M.P.
13.
12,
De W.
14.
13,
Simp.
15.
9, 1.4, Conj.
10.
16.
9, Add.
17.
16,
18.
10-1.7,
19.
18,
20.
19, D. N.
14
22,.
NZC
23.
(NAG)
24 .
(N-G)
9,
l
Taut.
21,
C.P.
8,
Conj.
22,
(GUN)
C.P.
Impl.
20,
21.
D.S.
23, Equiv.
C.P.
25.
4-24,
26.
HYP.
27,
FIYP.
28,
3,
29.
28,
30.
27-29,
31.
HYP.
32.
33.
EIYP.
Reasoning
34.
32-33,
Tat
(Es)
36
37,
39
40
M.P.
M.P.
26,
C.P.
as in 11-17
C.P.
Reasoning
35,
38
27,
31-35,
- (GZbT)
(T-C)
%a( 7'ZG)
[
Cs(
NZG)
l
[cCa(
‘IEG)
]
Conj.
36,
30,
37,
Equiv.
26-38,
]
as in 1.9-21
C.P.
25,
C.P.
39,
Conj.
sis -C is applicable. There is conformity
to the criterion of asymmetry.
Limitation
of production
by producer
cells may be established on a partially observational basis by two considerations.
Phytoplankton
---I-.--.--Deduction
[~43(Tx)
___._--_---Deduction
]
3
1.
IIYP -
2.
IIYP *
3.
IIYP IIYIYPm
3, Simp.
4*
5.
4, 2, M.P.
6.
5, D.N.
7.
6, Imp'L.
[ ~$93)
2.
W
3.
LWD(TGG) ] - [C=J(NGG) ]
I-IYP 1, Corn.
4.
Wza(TX)
T:G
lr
_~_
2
1.
5.
I-
--.. -.-- -
203
limitation
FYP.
-
The first is that off northwest Africa loss of
cells to grazing and sinking may be inferred
from the occurrence of ammonia. Rapid
excretion of ammonia by grazing copepods
is attested by many studies (e.g. Beers
1964; Butler et al. 1969; Corner et al. 1965;
Harris 1959; Martin 1968; Redfield and
Keys 1938). But ammonia occurred not
only in the homogeneous, near-surface
layer, 40-60 m deep, but well below to 200
m. Cells counted at four stations in the
nonupwelling
region totaled 287 and 270
per 200 cm3 at depths 0 and 40 m, were less
at 100 m, 111 per 200 cn-?, and were ncgligiblc at 400 m, 11 per 200 cm3. So cells
were lost, by sinking, from the homogencous layer, and their consumption by copepods at 100 m and below would account
for ammonia there, This ammonia would
prevent net loss of ammonia from the homogeneous layer by vertical mixing, and the
much greater concentration of nitrate below
the layer would add to the upper layer by
vertical mixing and so offset losses of particulate nitrogen due to sinking, in the
manner envisaged by Dugdale (1967) and
Eppley et al. ( 1973).
A second consideration is useful in placing limitation
of production by producer
cells on a partially observational basis. Off
northwest and central Africa, ccl1 numbers
appeared to be fairly uniform from place
to place and this uniformity suggests that
cell numbers should likewise have been
fairly uniform from time to time.
The first consideration is incorporated
into a third deduction as ‘L’ and the second
as hypothesis 3 ( deduction 3). The clauses
of the hypotheses are:
2, De M.
8.
7, 4, M.P.
9.
8, 4, Conj.
10.
1, 9, M.P.
11,
3, 10, M.P.
I 2,
II,
13.
12, Simp.
14 I
4-13,
corn.
C.P.
__________ -.- .__.._--_----. _-.-- . __------_ -- . --
A = ‘prior, rcsidcnt cells had absorbed
nutrient bcforc the survey’;
L = ‘prior, resident cells had produced
cells lost to grazing and sinking’;
0 = ‘prior, resident cells had produced
the presently observed, resident cells’;
R = ‘number of observed, resident cells
limited the number of cells subsequently
produced and remaining’;
T = ‘number of observed, resident cells
limited the number of cells subscqucntly
produced-the?+lost to grazing and sinking.’
(This is virtually the same definition of T
as for deduction 1. )
The
concluding
conditional,
L 1 T,
reads ‘if prior, resident cells had produced
cells lost to grazing and sinking ( L ) , then
the number of obscrvcd, resident cells
limited the number of cells subsequently
produced-then-lost
to grazing and sinking
(T)‘. Why is ‘if’ used in ‘if prior, resident
cells. . .’? The reason is that ammonia may
have been added to the water by rain (Menzel and Spaeth 1962) to the north and east
of the survey area (for it hardly ever rains
in the Canary Islands region)
v
, and that that
water may then have drifted into the survey
area. This is conceivable, but it could
never be wholly true, because of the cverpresent grazers. Biologists seem to favor
the biological origin of -ammonia, and thus
204
IIulburt
-- - __-___ __._
Deduction
I. T+bG)
2. G=@T)
4
-_Deduction
.C)
‘L’.%C
HYP HYP.
5
IIYP.
IlYP -
3.
HYP -
4.
r
J.
IIYP *
1, 4, M.P.
6.
5, 3, M.P.
[~\,(%TvG)vQ(%GvT)
7.
4-6,
[&sT.~G)v(~vLG~~T)I~~F
6, De M.
8.
[(T-~G)v(G-~T)I~~F
7, D.N.
9.
BYP2, 8, M.P.
(T.%G)v(C.%T)
2, Add.
10.
9, 3, M.P.
'LF
8,
Il.
8-10,
12.
7, 11,
13.
12,
14. Fx(TIG)
3-l.3,
Fzf
b[
l
(WI’)
(CS)
1,
]
2
c.P.
C.P.
11.
Equiv.
3, Trans.
*Ii?
"[(%TvG)*(+GvT)]~F
4, Impl.
l=P
5, De M.
9, M.P.
2-10,
c. P.
Conj.
Equiv.
C.P.
the USC of ‘if’ would be to stress the biological origin as evidence of grazing and
loss of cells,
Resident cells were predominantly
coccolithophorids,
which is to say they were
predominantly
round in form (the two
dinoflagellate species, K. rotund&urn
and
G. punctatum, are globular, thus nearly
round).
So to rcfcr to rcsidcnt cells off
northwest and central Africa is to include
reference to round cells. The incorporation
of ceil form into the nutrient cycle is accomplished in deduction 4 where the only
new claus6 is
F = ‘cells wcrc predominantly
form’.
(‘ix)
(‘bG).
round
in
Thus, ‘if cells were predominantly round in
form’, then the asymmetric nutrient cycle
with limitation by resident cells prevailed.
And the contrapositive of this is: if the nutrient cycle did not prevail, then cells were
predominantly nonround in form, “(T 3 G)
One way in which the
1 -F (Trans.).
breakdown of sequences of limitation
in
nutrient cycling could happen is by lost
cells not limiting nutrient gained, -G, with
resident ceIIs still limiting cells lost, T, to
give T - -G. A second way in which the
breakdown could happen is the converse,
G e -T. The logical conscqucnces of the
first way that breakdown could occur arc
cxamincd in deduction 5. In the conclusion
-P is ‘cells were not predominantly round’,
referring, of course, to diatom cells, which
are cylindrical, square, rectangular, discoid,
almost any shape but round. These cells
were dominant adjoining the upwelling
area off northwest Africa (Fig. 2) and in
the upwelling
arca off southwest Africa
(Fig. 4)) where the only round cells were
those of C. hudeyi and G. oceanica. But in
the northern part of the area of Fig. 3,
thcrc ~~2sa mixture of round and not-round
cells, since in addition to the coccolithophorcs just mentioned the undetcrmincd
flagellate and G. punctatum are approximately round. Still, as compared to the
southern part of Fig. 3, the proportion of
not-round cells was clearly much greater.
The alteration of G in the nutrient cycle
to -G, ‘cells lost to grazing and sinking did
not limit nutrient gained’, indicates the addition of new nitrogen from below the upper homogeneous layer of water. Dugdale
( 1967) called ammonia regenerated nitrogen, meaning that ammonia is produced in
situ from plankton. He called nitrate new
nitrogen, meaning that it is an additional
amount from below the homogeneous surface layer. IIc measured ammonia and nitrate uptake and found in near-surface water at Bermuda a predominance of ammonia
uptake, the ratio of nitrate to nitrite plus
plus ammonia uptake being 8.3% bctwecn
Scptcmber and January. Gocring and Dugdale (1964) found ammonia uptake 10
Phytoplankton
times greater than nitrate uptake in NovtimFinally,
Menzel and
her at Bermuda.
Spacth (1962) found an cxccss of ammonia,
amounting to as much as or more than 1
,ug-atom N liter- 1, throughout the year at
Bermuda.
One might suspect an enrichment with
new nitrogen, nitrate, in the arca adjoining
upwelling
off northwest Africa ( Fig. 2)
and in the much larger carea of abundant
cells in the northern part of the area shown
in Fig, 3, where diatoms and a flagellate
often dominated. It is rtiasonable to wonder
whether the asymmetric sequcnccs of limitation embodied in T = G were partially
broken down here by intrusion of nutrient
from below. But in the upwelling arca off
southwest Africa (Fig. 4) it is plain that
large amounts of new, nitrate nitrogen occurred. This was probably the dominant
form of assimilable nitrogen; in a similar
area off Peru, Remsen ( 1971) found that
nitrate was 69% of nitrate + nitrite + ammonia -t- urea. Thti breakdown of the sequences of limitation in which cc11 conccntration was the source of limitation would
seem assured. Further evidence for the
breakdown is found in the probable transport of nutrient from below upw‘ard, along
nearly vertical density surfaces-as
elegantly illustrated by Hobson ( 1971). After
assimilation to organic matter, the nutrients
transported upward are thought to sink or
to bc carried down by grazing copepods
and their predators everywhere within the
upwelling region. Such sinking, with attcndant decomposition, and downward transport, with attendant respiration, would account for the excessive depletion of oxygen
at 100-200 m in Fig. 5. This low oxygen
water is then supposedly carried by the
general circulation throughout the: South
Atlantic gyre, and is now considered the
0rigi.n of the oxygen minimum
layer
throughout the South Atlantic Ocean (Bubnov 1966; Menzel and Ryther 1968, 1970).
Coverage of such a vast area indicates an
active transport through the upwelling region, suggesting in turn a relatively minor
role of in situ cycling of nutrient thcrc.
The breakdown of the sequences of limi-
limitabion
205
tation and the consequent minor role of nutricnt cycling symbolized by -G leads to an
equivocal position. This stems from a cons&ration of the great differences in species
cell number from place to place in the upwelling region, which suggests similar large
diffcrcnces from time to time, so that limitation of subsequent resident species concentra tions by prior resident concenrtations
should be minor. Now, resident cells might
limit subsequent abundances in the upwelling region just as they did in the nonupwelling region, thereby limiting cells producedthen-lost, a conceivable though unlikely
possibility.
But if resident cells did limit
cells produced-then-lost,
T, and this loss of
cells did not limit nutrient gained, “G, then
cells were not predominantly round in form,
-F. -G and -F represent what was actually the cast. The statement (2’ * “G) 2 -F
in deduction 5 mixes, thcreforc, mere conccivability in T with actuality in -G and
-F. Such a mixing-an
equivocation-invalidates ( T . *G) 2 -F as a viable statemcnt for describing what happened. The
equivocal element is the word ‘cells’, which
is used in two voices (senses). In T ‘cells’
is used to rcfcr to ~11s that limit progeny
by growing slowly; in -G ‘cells’ is used to
refer to cells whose great spatial differences
suggest a capability of growing fast.
Scquenccs of limitation
in nutrient cycling, it may bc remembered, can break
down when tither T . -G or G . -T apply,
,And so a deduction similar to deduction 5,
but in which the altcrnativc
hypothesis
G* -T is used in the second step, would
lead to the conclusion (G * -T) 1 -F by
the same reasoning as that used in deduction 5. Figure 4 shows a large, dominating
abundance
of the rectangular
diatom
Hemiaulus hauckii at one station in the
northern part of the arca beyond any effect
of upwelling, though it occurred at very
low abundance at several other stations,
Thus at this northern sta.tion prior resident
cells did not limit abundance of thcsc observed rectangular ~11s: both -T and -F
were true. Possibly where I-1. hauckii was
so abundant, it was not grazed. Thus one
cannot know whether cells were lost to
206
Hulburt
grazing and sinking when the abundance
of H. hauckii exhibited no uniformity;
one
cannot know whether cells lost limited the
nutrient gained when uniformity of abundance did not prevail, G is suspected of
being false. Its falsity stems from its reference to cells (round ones) that were
uniform from place to place, whereas in
-T the cells referred to were not uniform
spatially.
Thus (G - “T) 2 -I? is not a
viable statement for describing what happened.
The fault lies in using a conceptual framework for both regions wherein T and G refer to different sorts of cells-where
there
is equivocation in the use of the word ‘cells’.
Beyond this the fault lies in using the converse of the conceptual framework of the
nonupwelling
region for the upwelling region and for the aberrant station where N.
hauckii was abundant. The fault lies in
switching from F 1 (T = G) to “(T = G) 1
-F in the hope that the statement dcscribing what happened in the nonupwelling regions needs only to be negated to obtain a
statement describing what happened in the
upwelling region and the aberrant HemiauZus station. Is there a conceptual framework
applicable to both regions-that
is, is there
a statement applicable to both in which no
word is used equivocally? In the following
sections such a statement will be found. I
will show that for such a statement to be
applicable to both regions the statement
must be of a type that cannot be negated.
Nonprevention
and limitation
Consider, as an example, a pair of species from the U. tenuis group of species in
Fig. 2. One species of the pair did not prevent the occurrence of the other where they
co-occurred. Consider also the species in
the upwelling region off southwest Africa
(Fig. 4)- one spccics did not prevent the
occurrence of another where they co-occurred. Take, as well, species of both kinds
intermixed, as among the Cape Verde Islands and southward (Fig. 3) : a species
of one kind was not prevented from occurring by a species of the other kind. So, in
general it may bc explicitly said ‘if it was
not the cast that
and species Y did
the occurrence of
the occurrence of
-(X
species X occurred (X)
not co-occur (WY), then
species X did not prevent
species Y (wP)‘:
s-Y>
1-P.
(9)
By successive application of De Morgan’s
theorem, the rules for double negation and
for material implication, this statement can
be transformed to
(X 1 Y) 3 -P.
(10)
Thus, ‘if species X occurred, then Y cooccurred, and if this was the case ‘then X
did not prevent Y from occurring’, But the
first ‘if and then’ clause makes a weak contextual claim-if
X should occur, then why
should not Y co-occur. For, when measured
there was excess ammonia or nitrate, in all
samples, for X and Y to share at all times, a
suitable context for co-occurrence.
The last statement covers contextual relationships other than that of co-occurring
species. Cells did not prevent the occurrence of excess nutrient they would need.
Grazers and other decomposers did not
prevent the occurrence of the cells they
would supposedly require. These relationships are contextual, for they conform to
the colloquial locution ‘if X why not Y-if
cells should occur, then why should not ammonia or nitrate co-occur in excess?
Consider ammonia in the nonupwelling
region off northwest Africa. ‘If resident
cells occurred (D), then excess ammonia
co-occurred (iW>‘, and if this was the cast
‘then cells did not prevent excess ammonia
from occurring (-P)‘.
Next, ‘if resident
cells had not limited the cells producedthen-lost to grazing and sinking (T)‘-that
is, if resident cells had not limited production by possessing an inherently low growth
ratc- ‘then they would have prevented the
occurrence of excess ammonia (P)‘. Assuming the contextual relation, D 2 M, a brief
deduction shows that limitation by resident
cells is the consequence (deduction 6).
Statement -T 1 P of step 2 of deduction
6 seems to be reasonable. Yet is it? It is
to be doubted on two grounds. Experimcnts b,y Parsons and LeBrasseur ( 1970)
Phytoplankton
Deduction
207
limitation
Deduction
6
7
1.
(D-;M)~w
IIYP.
1.
(D~M)zII
ITYP.
2.
%TZJP
IIYP.
2.
H=T
HYP -
3.
D34
HYP-
3.
D3X
HYP.
4.
QP
1,
3, M.P.
4.
H
1,
5.
T
2, 4, M.P.
5.
WT
2, 4, M.T.
6.
T
5, D.N.
I=
6. I (DIM)XT
3-6,
____-.-
7.
b (DIM)~T
C.P.
3-5,
3, M.P.
CA?.
----~
and McAllister
(1970) show that grazing
does not occur below a threshold conccntration of phytoplankton
and Parsons and
LcBrasseur (1970) give a range of threshold concentrations of 40-190 lug C liter-l,
which approximates but is slightly more
than the range of 30-134 pg C liter-l of particulate carbon in the near-surface (O-60 m)
layer of the’ section off northwest Africa. So
the clause ‘if resident cells had not limited
cells produced-then-lost to grazing and sinking’ would be wrong, if resident cells were
too sparse to stimulate’ any grazing at all. In
addition, there is always the doubt whether
the cells we counted were the ones grazedperhaps smaller ones, as indicated in some
of the experiments of Sheldon et al. ( 1973))
or perhaps larger ones, Ceratium for example, were the primary food of the grazers.
Still, these doubts are merely doubts.
The second ground for doubting -T 1 P
is that it is discordant with the previous
statcmcnt, (D 1 M) 1 -P. First, it is a
matter of mere conceivability
that ‘nonupwelling cells had no,t limited production’,
-T, that, in effect, cells of H. hauckii: or
other rapidly growing spe’cies would be
abundant throughout the nonupwelling
region as they wcrc at the southern part of
the area of Fig. 2. For this would bc a very
unlikely occurrence, when species of the
U. tcnuis group, C. huxleyi, and G. oceanica
arc so likely to occur repeatedly at low
concentrations throughout the nonupwelling area. Second, it is a matte’r of mere conceivability that cells of any species whatsoever ‘would have prevented the occurrence
of a11 excess of assimilable nitrogen’, P.
This would be’ equally true for any other
nutrient. If cells absorbed all excess, then,
certainly, they would not exist for long. It
is doubtful, too, that complete absorption
of excess could ever happen. So, to say
that resident cells would have’ prevented
the occurrence of cxccss ammonia is ,to conceive something happening which it is very
doubtful could happen. Thus the issue
hcrc is equivocal-using
a standard of actuality in ( D 1 M ) 1 “P, then a standard of
mere conceivability
in -T 1 P.
What is needed is a statement replacing
-T 2 P, which would permit only a standard of actuality and would exclude conceiving the nearly impossible.
Consider
this statcmcnt, ‘if it was not thd case that
resident cells occurred (0) and excess ammonia did not occur (-M ), then the cooccurrence of cells and excess ammonia
was harmonious (H )‘,
“CD . -M) 2 II.
(11)
This statement cannot be denied; for if the
co-occurrence of cells and excess ammonia
was not harmonious, then cells occurred
and excess ammonia did not. This absurdity
is shown by applying the rules for transposition and double negation to statement 11
to obtain
-H
2 (D - -M).
1W)
Deduction 6 is then transformed by replacing -P with II ( deduction 7). Thus, assuming the contextual relation ‘if cells occurrcd, then excess ammonia occurrcd’and the intent of saying ‘if’ in ‘if cells occurred’ is plainly to rule out what is conceivable, that they might not have occurred,
and to stress the actuality that they did
occur- assuming this contextual relation, a
208
Hulburt
harmonious relation, the consequence was
that ‘resident cells limited production of
~~11slost to grazing and sinking’.
Deduction
1.
(D=JI)S
IIYP.
2.
Co-occurrence
Consider the nonupwelling
and upwelling regions, Co:nsider o,nly the cells that
actually dominated in these regions, not the
cells that conceivab,ly could dominate but
actually did not dominate there. Consider
then the round, predominantly
coccolithophorid dominants of the nonupwelling
region and the predominantly not-round, predominantly dia tomaccous dominants of the
upwelling region.
a) ‘If excess nitrogen limited nonupwelling cells to small numbersi.e. prevented
them from being abundant (-W)-then
nonupwelling
cells were not abundant
(“B)‘.
b ) ‘If upwelling
cells were abundant
(B), then excess nitrogen did not limit upwelling cells to small numbers-i.e.
did not
prcvcnt them from being abundant (W)‘.
a) and b ) arc shown in statements 13
nncl 14.
-W 1 -B.
(13)
BI-W.
(14)
Thcsc statements can be joined by the rule
of conjunction:
6-W 1 “B) . (B 2 -W).
(15)
Statement 13 is falsified by cells belonging
to species of the U. tenuk group. They
were not prevented from being abundant,
because they did not respond to the large
amount of nitrogen of the upwelling region.
Thus statement 15, the conjunction of two
statements, one of which is false, is itself
false.
What is needed is a statement that holds
true for both nonupwelling
and upwelling
regions, such c’s ‘if resident cells occurred
(D), then excess nitrogen occurred (I)’
and if this was the cast ‘then the co-occurrence of resident cells and excess nitrogen
was harmonious ( II)‘:
(D’I)
III.
(16)
8
HYP.
2, De M.
3,
5.
6.
D.N.
4, Impl.
1, 5, M.P.
Saying ‘if it was the cast that ( D 2 I) ’ rules
out the conceivability
that resident cells
occurred and excess nitrogen did not occur
for in actuality ‘it was not the cast that
resident cells occurred and excess nitrogen
did not occur’, as shown in step 2 of deduction 8. ‘The co-occurrence oE resident cells
and excess nitrogen being harmonious’ (E-I)
was common to both nonupwelling and upwelling regions, to both small and large
amounts of cells and excess nitrogen (ammonia, nitrate), and to subsequent production of both small and barge amounts of
cells from observed resident cells and observed nitrogen.
It is necessary to state explicitly ‘co-occurrence of cells and cxccss nitrogen was
harmonious’. In this way the false predicate ‘were limited’ is avoided in ‘cells, occurring with small excess of nitrogen, were
limited’.
The false predicate ‘was prcvented’ is similarly avoided in ‘abundance
of cells, occurring with a small excess of
nitrogen,
was prevent&V.
These f alsc
predicates are, holwever, explanatory or informative. Without them one could point
to the occurrences of cells and nutrient resource, but not say anything about them.
l3ut these predicates arc false and should
be replaced in the logical model by the
prcdicatc ‘was harmonious’, which is true.
An inclusive
predicate
‘Were harmonious’ is an inclusive predicate, shown by means of the following
three cases. 1. Cells did not prevent excess
nitrogen, i.e. they were harmonious to cxccss nitrogen. 2. Cells lost were necessary
and sufficient for the occurrence of excess
Phytoplankton
nitrogen, because prior, resident cells produced the cells which were grazed and
which la.ter appeared as excreted nitrogen:
thus cells lost were harmonious to the occurrence of excess nitrogen. 3. Resident
cells were beneficial to, were harmonious
to, subsequent occurrence of excess nitrogen, The first case applies to upwelling
and nonupwclling
regions; the second and
third cases apply only to the nonupwelling
region. But with ‘cells’ and ‘excess nitrogcn’ exchanged-which
can easily be tried
(replacing
‘were’ by ‘was’)-these
three
cases apply to both regions.
No predicate with a greater generalizing
capability or greater ecological applicability
is likely to be found than the predicate
‘were harmonious’ in ‘cells and excess nitrogen were harmonious’.
Resume’
But to say that a consumer and a consumable resource, such as cells and excess
nitrogen, were harmonious to each other is
to ob,scure a peculiar and distinctive feature
of the plankton off the African coast. By
noting that resident cells in a nonupwelling
area did not respond to the added nitrogen
of an upwelling area, one can see that there
was more than enough nitrogen, and prcsumably other nutrients, for these nonupwelling cells. There was, it would seem, an
accumulation of nitrogen in the nonupwelling region.
It would stem natural to imagine that
the apparent accumulation of nitrogen in
the nonupwclling
region was added to by
decomposition
of cells produced by the
resident cells there. It is easy to imagine
that resident cells, in order to produce
these cells, withdrew an amount of nitrogen
equal to that added. What is distinctive
here is that the resident cells are not a constituent in the symmetry of the cycle of
gain and loss. They stand outside the cycle
because the added nutrient, instead of coming from them, comes from the cells produced and then later lost to decomposition.
But they limit the rate of this cycle by the
rate at which they arc maximally capable
of producing those cells that arc lost to de-
limitation
209
composition. One gets two things in resident cells, the cell-producing
agency that
limits the cycle and the nutrient-withdrawing agency that balances the cycle.
When one observes these resident cells,
one sees round cells. I have stuck to “round’
because .one actually sees something round
or sees roundness directly (depending on
which philosopher is read). It seems to me
that since I have made such a fetish of
sticking to what is actual, I had better stick
to what was actually seen: I doubt that one
ever sees a coccolithophore
or a diatom.
Roundness is a mark of their physiological
status of not responding to added nutrient.
The shift from round, unresponsive cells to
predominantly
not-round, responsive cells
paralleled a shift from a small amount of
available nitrogen in the nonupwelling
region to a large amount of available nitrogen
in the upwelling regions. In addition, the
change from a small concentration
to a
large concentration of cells paralleled the
change of increased availability
of nitrogen. In neither case does one have a simple experiment showing dependence on nitrogen, because the physiological status of
the experimental
material, so to speak,
changes. So ond camrot say that, when the
balanced nutrient cycle bsreaks down in the
upwelling
region, limitation
of the cycle
by resident cells also breaks down, because
one is talking about a radically different
physiological kind of resident cell-an
opportunis tic kind that achieves marked
abundance in a very sporadic manner, Likcwise, it is impossible to point to the change
in abundance of cells from nonupwelling
to upwelling
regions with the intent of
showing dependence on the change from
supposedly limiting to nonhmiting nutrient
conditions, because again the physiological
type of the cells is so different in these rcgions.
There are two exceptions to the classification of cells into round, unresponsive
ones and predominantly not-round, rcsponsive ones : the species C. hux2eyi and G.
oceanica. These two were not abundant in
the nonupwelling
region but were moderately abundant at three locations in the up-
210
Hulburt
welling region. Here one does have a simple experiment:
if added nitrogen in the
upwelling region produced the abundance
of these species, then the levels of nutrients
origimally present in the nonupwelling
region produced the original abundance of
these species, For those who favor the concept of limitation,
the second ‘produced
would be changed to ‘limited’. To me, this
seems to mix t&o quite different concepts,
that of production and that of limitation,
It would stem clearer to adhere to one concept,and the more reasonable one here is
that of production.
It is more reasonable
particularly because nitrogen would be simply productive instead of contradictorily,
both productive and preventive of production.
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Submitted:
Accepted:
25 March 1975
3 November 1975