Download Quasi K-Selected Species, Equivalence, and the

BULLETIN OF MARINE SCIENCE, 33(2): 197-212, 1983
QUASI K-SELECTED SPECIES, EQUIVALENCE, AND THE
OCEANIC COCCOLITHOPHORID PLANKTON
Edward M, Hulburt
ABSTRACT
Coccolithophore species, other than Emiliania hux/eyi and Gephyrocapsa oceanica. make
up a group of about 20 species in the western North Atlantic and the Mediterranean, Most
of the species are the same in both places and provide the same ordered decrease of abundances
in both places, suggesting an equilibrium condition, Thus we may say 'if, given any species,
one species belongs to a diverse cocco litho ph ore group, then it occurs under equilibrium
conditions and occurs in the deep ocean'; this implies 'if the given species does not occur
under equilibrium conditions or does not occur in the deep ocean, then it does not belong
to such a diverse group,' Along the coast of Colombia and Ecuador in the Pacific growth
conditions result in very uneven plankton concentrations indicating lack of equilibrium and
the diversity of coccolithophores is reduced, certifying 'if the given species does not occur
under equilibrium conditions, then it does not belong to a diverse coccolithophore group.'
In the Gulf of Persia the water is quite shallow, making possible stranding of cocco litho ph ores
on the bottom during the unstratified winter period, and just a very few coccolithophore
species are present. So this certifies 'if the given species does not occur in the deep ocean,
then it does not belong to a diverse coccolithophore group.'
The approach of the following study is to show ecological relationships by logical
equivalence, Where such relationships have a comparative aspect, equivalence
provides the correct way that such relationships can be reported, Any non-equivalent statement of relationships would be incorrect. What ecological relationships,
then, would be of general interest for the application ofthe equivalence criterion?
Guillard and Kilham (1977) extend the r-selected, K-selected distinction of
Pianka (1970) to the phytoplankton. Their intent is to extend terrestrial ecological
concepts to plankton ecology. Thus, K-selected phytoplankton species are in competitive equilibrium with one another at the carrying capacity of the ecological
system, producing only a minor progeny of new cells, which is enough to offset
grazing-sinking loss. But competitive equilibrium might mean that no species in
an equilibrium group can bring the concentration of a crucial nutrient into exact
adjustment with its demand, otherwise the species with the lowest concentration
demand (the lowest 1(,.) would reduce this nutrient to its level and exclude all
others. Or competitive equilibrium might mean that different demands of different
species are matched with different transient ratios of two nutrients, permitting
coexistence (Tilman, 1977). As a first option, a little reflection would seem to
advise that 'competitive' of 'competitive equilibrium' should be dropped. So
'quasi-K selected,' indicating equilibrium of coexisting species without competition, would then be avowed-otherwise
no equilibrium could occur until one
species had competitively excluded all others. Or, as a second option, drop 'equilibrium' and keep 'competitive' thus indicating competition of coexisting species
without equilibrium.
First Option. -If a given species belongs to a diverse, coexisting group, then it
is in equilibrium with others of the group. Let us take the oceanic coccolithophore
group of species-those
coccolithophores that prevail across deep, oligotrophic
stretches of ocean but decrease over shoal continental shelves (Hulburt, 1979).
So, (A), if a given species belongs to a diverse group, then it occurs under equilibrium conditions and occurs in the deep ocean. By logical equivalence, (B), if
197
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BULLETIN OF MARINE SCIENCE, VOL. 33, NO.2,
1983
this species does not occur under equilibrium conditions or does not occur in the
deep ocean, then it does not belong to a diverse group. We know from equivalence
what conditions imply a reduced diversity of the oceanic coccolithophorid group.
'B' is the ecological opposite to 'A'-but the reversed order in 'B' of the parts of
'A' (and the switch from 'and' to 'or') are vital to correct reporting.
Second Option. - Two coccolithophores, Emiliania huxleyi and Gephyrocapsa
oceanica, increase in abundance over shoal shelves and in upwelling regions, as
do so many diatom species (Marshall, 1969; 1971; Hulburt, 1976; Hulburt and
Mackenzie, 1971). These coccolithophores (and diatoms) are r-selected, nonequilibrium species, because they can produce an excess progeny of cells under
improved conditions. But E. huxleyi, at least, occurs everywhere and in association with the other coccolithophores in the Atlantic Ocean (Hulburt, 1976; 1979;
Hentschel, 1936; Marshall, 1966; 1968; 1969; 1971; 1978; Marshall and Solder,
1982; McIntyre and Be, 1967; Okada and McIntyre, 1979; Throndsen, 1972). So,
overall, if there is independence of E. huxleyi and G. oceanica, from the rest of
the coccolithophores, they must be competing with the others only in the obvious
sense of sharing nutrient. And likewise the rest of the coccolithophores should be
competing with each other in the obvious sense of sharing nutrient.
METHODS
Phytoplankton samples were counted alive soon after they were taken on all cruises except the one
to the Gulf of Persia. They were concentrated by centrifugation: first 90 em' were centrifuged in six
IS-em' tubes; then after removing supernatant, the tubes were refilled and again centrifuged; the
residual of the six, after supernatant removal, was transferred to one tube, which with enough added
sample to bring the total volume processed to 200 em' was centrifuged, the residual finally being put
on a slide under a rectangular cover slip for enumeration under standard light microscope. Most of
the coccolithophore cells observed were reliably identified to species. But often several undeterminable
coccolithophore cells were observed in any particular sample. So, at 36°N, 66°W there are first 372
identified and 24 unidentified cells, later 266 identified and 30 unidentified cells; between Bermuda
and Florida 371 identified and 10 unidentified cells; and in the Mediterranean 403 identified, 40
unidentified. If some of the unidentified cells are different species, then there would be considerably
more species than the approximately 20 species observed in each of the four cases, Taxonomic studies,
such as those of Okada and McIntyre (I 977), of Heimdal and Gaarder (1980; 1981), and Throndsen
(1972) present rosters of 50 or more species, undoubtedly both because scanning electron scope analysis
brings out species differences not visible by light microscope and because rare but different species
are sought.
Temperatures were taken by bathythermograph at the time of sampling, except at 36°N, 66°W when
the ship remained in the same place and except in the Gulf of Persia when temperatures were taken
several weeks earlier by reversing thermometers. Dates of the plankton survey in the Gulf of Persia
are 6-14 March 1977 and of the temperature survey 17-24 February 1977 (Brewer et aI., 1978),
Catalogues of Quasi-K-Selected Coccolithophores
A catalogue of average concentrations of coccolithophores except E. huxleyi
and G. oceanica shows an even and ordered decrease in concentrations in the
Atlantic (Fig. I) 12-17 October 1981 (Table I). A continuation of the survey, 1721 October, shows the same ordered decrease in abundance, with some shifts in
positions of names in the upper ranking. The names are mostly the same. The
range of concentrations is 1 to 92 cells/liter in the first part of the survey, 1 to 74
in the second part.
A section from Bermuda through Providence Channel and into the Straits of
Florida (Fig. 1) was made 2-6 November 1968. Table 2 shows nearly the same
ordered decrease in abundance. Again many of the names are the same as at 36°N,
66°W. And again there are some shifts in position in the upper ranks. The range
of concentrations goes a little higher, 2 to 148 cells/liter.
HULBURT:
COCCOLITHOPHORJD
PLANKTON
199
UNITED
SAUDI
ARABIA
Figure 1. Location of sampling. Upper left, the western North Atlantic Ocean. Upper right, the
Mediterranean Sea. Lower part of figure, the Gulf of Persia. Right inset, the Pacific Ocean adjoining
Colombia and Ecuador.
A repetition of the ordered decrease in abundance and of the names of the
western North Atlantic is provided by sampling from the Mediterranean Sea 1825 September 1970 (Table 2). But some names are new (shown by asterisks),
indicating an appreciable difference, though a small one, between the Mediterranean and the Atlantic. Such a difference is reasonable in view of the isolation
of the Mediterranean from the Atlantic. But a repetition of the same range, I to
110 cells/liter, emphasizes an essential likeness of the Mediterranean to the Atlantic.
These four similar cases have about 20 species, mostly the same, for 266-403
cells counted in about 3f4 of a liter total water searched. Each species is a member
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BULLETIN OF MARINE SCIENCE, VOL. 33, NO.2,
1983
Table 1. Northern Sargasso Sea, at 36°N, 66°W. Average concentrations
cells/liter, except Emiliania huxleyi and Gephyrocapsa oceanica
12-17 October 1981
Discosphaera tubifera
Syracosphaera pulchra
Umbellosphaera tenuis
Calyptrosphaera oblonga
Umbilicosphaera hulburtiana
Umbellosphaera irregularis
Cyclococcolithus leptoporus
Thoracosphaera heimii
Helicosphaera hyalina
Helicosphaera carterae
Syracosphaera mediterranea
Helladosphaera aurisinae
Rhabdosphaera stylifer
Syracosphaera dentata
Homozygosphaera spinosa
Rhabdosphaera ciaviger
Helladosphaera cornifera
Acanthoica acanthifera
A nthosphaera robusta
Rhabdosphaera hispida?
Ophiaster hydroideus
of all coccolithophorids
in
17-21 October 1981
92.2
76.7
57,2
42.9
37.7
29,9
28.6
26.0
15.6
13.0
11.7
11.7
10.4
5.2
5.2
3.9
3.9
1.3
1.3
1.3
1.3
74,3
62.9
58.6
38,6
22.9
Syracosphaera pulchra
Discosphaera tubifer
Cycloccolithus leptoporus
Umbellosphaera tenuis
Umbilicosphaera hulburtiana
Calyptrosphaera oblonga
Syracosphaera mediterranea
Helicosphaera carteri
Anthosphaera oryza
Thoracosphaera heimii
Umbellosphaera irregularis
Halopappus adriaticus
Helicosphaera hyalina
Syracosphaera dentata
Deutschlandia anthos
He/ladosphaera aurisinae
Rhabdosphaera stylifer
Rhabdosphaera hispida?
Michaelsarsia Jalklandia
18.6
15.7
15.7
15.7
14.3
10.0
8.6
7.1
4.3
4,3
4.3
1.4
1.4
1.4
12-17 Oclober.-21 species, 372 identifIed cells counted. 750 cm' in all searched. The 15 samples taken, each having 50 em' searched,
were from 0, 20, and 60 meters each day usually. 1.3/liter = I countcd ccll. Unidemifed cells = 24.
17-21 October.-19 species. 266 identified cells counted. 700 em' searched. The 14 samples. 50 em' searched each, were from 0.20,
and 60 meters each day always. 1.4/liter = I counted cell. Unidentified cells = 30.
Table 2. Bermuda to Straits of Florida 2-6 November 1968; Mediterranean Sea 19-25 September
1970. Average concentrations of all coccolithophorid species in cells/liter, except Emiliana hu.xleyi
and Gephyrocapsa oceanica
Bermuda to Florida
Umbilicosphaera hulburtiana
Discosphaera tubifer
Cyclococcolithus leptoporus
Umbellosphaera irregularis
Umbellosphaera tenuis
Calyptrosphaera oblonga
Syracosphaera pulchra
Syracosphaera mediterranea
Umbilicosphaera mirabilis
Syracosphaera dentata
Rhabdosphaera stylifer
Helicosphaera carterae
Thoracosphaera heimil
Helladosphaera cornifera
Acanthoica acanthifera
Pontosphaera syracusana
Acanthoica coronata
Halopappus adriaticus
Anoplosolenia brasiliensis
Mediterranean
148.0
116.8
72.0
54.4
51.2
38.4
35.2
30.4
20.8
11.2
11.2
8.0
4.8
4.8
3.2
1.6
1.6
1.6
1.6
Umbellosphaera tenuis
Calyptrosphaera sphaeroidea*
Cyclococcolithus leptoporus
Calyptrosphaera oblonga
Discosphaera tubifer
Helladosphaera cormlera
Rhabdosphaera hispida?
Syracosphaera pulchra
Syracosphaera bifenestrata*
Pontosphaera syracusana
Rhabdosphaera claviger
Rhabdosphaera styliJer
Syracosphaera mediterranea
Syracosphaera dentata
Calyptrosphaera insignis?*
Helicosphaera carterae
Rhabdosphaera multistylis*
Thoracosphaera heimii
Helicosphaera hyalina
Pontosphaera discopora*
Ophiaster hydroideus
Sea
110.4
93.1
82.4
57.2
30.6
29.2
23.9
18.6
15.9
9.3
9.3
8.0
8.0
8.0
6.6
6.6
6.6
5.3
4.0
1.3
1.3
Bermuda-Florida. - 19 species. 371 identified cells counted. 627 em' search. The 19 samples, each with 33 em' searched, were taken
from the surface. U nidentifJed cells = 10.
Mediterranean Sea. -21 species. 403 identified cells counted. 750 cm' in all searched. The 15 samples taken, each having 50 cm'
searched, were from 0, 50. and 100 meters at 5 stations shown in Figure I. 1.3/liter = I counted cell. Unidentified cells ~ 40 .
• Species not encountered in the Atlantic Ocean.
HULBURT: COCCOUTHOPHORID
PLANKTON
201
of a diverse group of species, let us suppose. If it is such a member, then, let us
say, it is under equilibrium conditions and occurs in the deep ocean. This is a
hypothesis, because of the initial 'if and the follow-up 'then'. Tentatively, belonging to a diverse group is confirmed by the 20 species in each place in ordered
ranking. The ranking not changing appreciably at 36°N, 66°W over a IO-day period
lends an element of confirmation to species being in equilibrium conditions there.
The samples did come from deep ocean water, in the Mediterranean as well as
in the Atlantic: confirmation is clear on this point. The next move will be to
develop this hypothesis through equivalence.
Equivalence
A population of a given species may be said to be a single entity at 36°N, 66°W
from 12 October through 21 October. But a population of the same species from
13 years earlier westward from Bermuda might be thought of as a different population, a different entity. And a population from the isolated Mediterranean
might best be considered still another population of the same species. In order to
have uniformity of treatment all four cases of Tables 1 and 2 will be considered
to provide for each mentioned species separate populations. Of course, there are
many more species populations. So, limiting consideration just to coccolithophores, we say 'given any species population x' -which is shown by '(x)'. Then
the hypothesis previously mentioned may be expressed now with the help of the
following abbreviations:
'Dx'-'x is a member ofa diverse coccolithophore
'Ex'-'x occurs under equilibrium conditions;'
'Ox' - 'x occurs in the deep ocean.'
group;'
The subject of the clause, 'x', comes after the predicates 'D', 'E', and '0'. Then,
joining a clause beginning with 'if with one beginning with 'then' by '::J' and two
'and-connected' clauses by'.' we have (confining consideration to coccolithophores
minus E. huxleyi and G. oceanica in 'D'):
(x)[Dx ::J (Ex. Ox)],
(l)
'given any species population x, if it, x, is a member of a diverse coccolithophore
group, then it, x, occurs under equilibrium conditions and it, x, occurs in the deep
ocean.' Briefly, 'any species population belonging to a diverse coccolithophore
group occurs under equilibrium conditions and occurs in the deep ocean.' Now
'y', 'u', 'v', or any other letter at the end of the alphabet could of course have
been used instead of 'x'. But denial 'not', shown by '~', and 'or', shown by 'v',
radically alter the total situation. We have:
(y)[Dy ::l (Ey . Oy)] ::J (x)[(~ Ex v ~Ox) ::J ~ Dx],
(2)
which says' if any species population belonging to a diverse coccolithophore group
occurs under equilibrium conditions and occurs in the deep ocean, then any species
population not occurring under equilibrium conditions or not occurring in the
deep ocean does not belong to a diverse group.' What is now crucial is 'y' and
'x'. There is now a point in having these two letters to refer to all the populations,
in the case of'y', which are D, E, and 0, and to refer to all the opposite populations,
in the case of 'x', which are not E or not 0 and consequently are not D.
The next move is arresting - first putting '(x)' out in front of the whole expression
202
BULLETIN OF MARINE SCIENCE, VOL. 33, NO.2,
1983
(in braces) and then changing '(y)' to '(3y)', meaning 'there is a species population y':
(x)(3y){[Oy ::) (Ey. Oy)) ::) [(-Ex
V
-Ox) ::) -Dx)} ,
(3)
This says that given any species population 'x' there is a species population 'y'
such that if '[... j' then '[ ... j'. We can drop all but one of the 'x' populations in
'(x)', since they are all alike, and work with just one 'x'. Further, we can substitute
'x' for 'y' and have, instead of two populations 'x' and 'y', just one 'x' population
throughout (Quine, 1972). Now, letting 'x' refer to one of the species populations
of Tables 1 and 2 in the first part of the following expression, we have this same
'x' behaving in a supposed opposite way in the second part of the expression:
[Dx ::) (Ex. Ox)) ::) [(-Ex v -Ox) ::) - Ox).
Expression (4) does what our common sense instinctively wishes-using
of 'x' to suppose the opposite of what we observe.
Expression (4) makes just as good sense in reverse:
(4)
one value
[(- Ex v -Ox) ::) - Dx) ::) [Ox::) (Ex. Ox)).
(5)
Letting the two bracketed parts of (4) be 'A' and 'B', the concept of equivalence,
wherein 'A' and 'B' are equivalent, comes to:
(A
::> B) . (B ::> A).
(6)
(The technical aspect of equivalence (at an elementary level) is given in the appendix.)
Quasi-K-Selected Species not in Equilibrium or in Shallow Water
The reason for entertaining the 'A' part of (4) 'if x is a member of a diverse
group, then x occurs under equilibrium conditions and x occurs in the deep ocean'
is that the 'x' can be supplanted by the names of species in Tables 1 and 2 to
confirm this part of the hypothesis (Hempel, 1970; Kahane, 1978). By supposition
and with one value of 'x' we pass from this 'A' part to the opposite 'B' part of
(4). Thence, confirming values of 'x' may supplant the single value of 'x' in 'if x
does not occur under equilibrium conditions or x does not occur in deep water,
then x is not a member of a diverse group.'
Let 'x' be supplanted by any of the species populations in Table 3, to confirm
the initial part of'B', 'x does not occur under equilibrium conditions.' Any species
population x not being in equilibrium is confirmed best by the behavior of the
responsive, r-selected species, Emiliania huxleyi, Gephyrocapsa oceanica, and
several other species. If growth conditions are at equilibrium, then these species
undergo very little fluctuation; but if these species do undergo marked fluctuations,
then growth conditions are not at equilibrium. Table 4 shows E. huxleyi as evenly
distributed as the quasi-K-selected remaining coccolithophores at 36°N, 66°W,
between Bermuda and Florida, and in the Mediterranean. This is in a hydrographic
structure that has stratification either close to the surface, the Mediterranean, or
not close to the surface, the Atlantic (Fig. 2). But how differently E. huxleyi behaves
off Colombia, Table 5; how erratic it is from location to location! Also, Gephyrocapsa oceanica, not observed in the Atlantic samples, fluctuates some. But the
most dramatic fluctuation is that of the green flagellate, Bipedinomonas pyriformis.
Then, these species do undergo marked fluctuations and therefore growth conditions are certainly not at equilibrium. This is in a hydrographic structure with
HULBURT: COCCOLITHOPHORID
203
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BULLETIN OF MARINE SCIENCE. VOL. 33. NO.2.
1983
Table 3. Colombia and Ecuador 8-12 March 1969. The Persian Gulf 6-14 March 1977. Average
concentrations of aU coccolithophorids in ce1\s/liter, except Emiliania huxleyi and Gephyrocapsa
oceanica
Colombia and Ecuador
Cyclococcolithus leptoporus
Syracosphaera mediterranea
Umbilicosphaera hulburtiana
Acanthoica acanthifera
Syracosphaera pulchra
Helicosphaera carterae
Calyptrosphaera oblonga
Discosphaera tubifer
Anoplosolenia brasiliensis
Umbellosphaera tenu~
Umbellosphaera irregularis
Gulf of Pcrsia
37.5
25.0
15.0
12.5
12.5
7.5
5.0
5.0
Calciosolenia murrayi
Anoplosolenia brasiliensis
Ophiaster hydroideus
Anthosphaera oryza
Braarudosphaera bigelowii
Acanthoica acanthifera
Umbilicosphaera hulburtiana
180.0
4.3
3.7
2.4
1.4
0.6
0.5
4.1
2.5
2.5
Colombia and ECI/ador. - LI specics. 43 cclls counted. 383 cm' scarchcd. The 12 sampLcs takcn, II of them with 33 cm' searched,
were from the surface. 2.Sfliter = I counted cell.
Gulf of Persia.-7 species. 253 cells counted. 1,641 emJ searched. The 31 samples taken, with the amount searched in each sample
ranging from 10 emJ to 100 emJ were from the surface, except as noted in Table 5.
stratification close to the surface, allowing, at any rate, non-equilibrium growth
conditions.
In the Gulf of Persia, Table 5, E. huxleyi fluctuates only slightly more (from
60 to 0 per 66 cm3) than it does in the Atlantic. G. oceanica goes from 138 to 0
per 66 cm3, a bit more fluctuation than E. huxleyi's. There are a few abundances
of several other species, two diatoms (Nitzschia and Guinardia) and the bluegreen Trichodesmium. Therefore, maybe there is no equilibrium. If the fluctuations of these species had been more marked or when marked had occurred more
frequently, we could have decided for non-equilibrium. But such a decision does
not seem justified. However, decision for non-equilibrium is not needed. Thus,
let 'x' be supplanted by any of the species populations in Table 3, to confirm the
second part of B, 'x does not occur in deep water.' For, either x is not under
equilibrium conditions or x does not occur in deep water-either
one, and just
one, is enough to imply the concluding third part of 'B'. And clearly the Gulf of
Persia is fairly shallow, no more than 50-60 m (Fig. 3), and the species populations
in such shallow water certainly confirm the second part of B.
Finally let 'x' be supplanted by any of the species populations in Table 3 for
populations off Colombia and Ecuador and in Table 3 for populations in the Gulf
of Persia. The fewer species off Colombia, 11, and particularly in the Gulf of
Persia, 7, confirm the final, third part of'B', 'x is not a member of a diverse group.'
Off Colombia less water, 383 cm3, was searched for species, it is true, than in the
Atlantic and Mediterranean, but this does not make much difference. For, at 36°N,
66°W 19 species were found in the first 400 cm3 searched, 21 species in the first
750 cm3 searched, and 26 species in the whole 1,450 cm3 searched. In the Gulf
of Persia about the same amount, 1,641 cm3, was searched as in the whole of
36°N, 66°W, but only 7 species were found. One of these is peculiarly abundant,
as if it is a responsive species, somewhat like E. huxleyi and G. oceanica. But the
other six are very low in abundance, telling us that loss of diversity is loss in
abundance.
Stranding
An hypothesis put forward in a previous paper (Hulburt, 1979) is that if coccolithophores (except E. huxleyi and G. oceanica) plus several dinoflagellates (such
HULBURT: COCCOLITHOPHORID
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HULBURT: COCCOLITHOPHORID
PLANKTON
207
as Oxytoxum) get stranded on the bottom when they are carried into shallow
western Atlantic shelf water, then they decrease in concentration over these shelves.
Confirming data for 4 shelf areas are given in Hulburt (1979). Kling (1975), too,
finds a less diverse cocco litho ph ore flora in shallow Honduras water than Throndsen (1972) finds in adjoining deep Caribbean Sea water. To achieve decrease via
stranding, they must grow slowly enough not to make up the stranding loss. By
contrast, species such as E. huxleyi and diatoms in shallow shelf waters obviously
more than make up any presumed stranding losses, because these species are
usually more abundant over continental shelves than in the deep ocean beyond
(Hulburt, 1968; 1979; Hulburt and Mackenzie, 1971; Hulburt and Corwin, 1972).
Stranding can account for the fewer coccolithophore species in the shallow Gulf
of Persia.
Stranding by contact with the bottom through vertical mixing, as well as sinking,
may occur in winter in the Gulf of Persia, since the isotherms in Figure 2 indicate
very little stratification then. In summer the surface water is lOoC warmer than
the bottom water (Emery, 1956), so stranding would only occur as a result of
sinking then.
There is no real alternative to this stranding hypothesis. It is unlikely that
grazing reduces coccolithophores other than E. huxleyi more than E. huxleyi and
diatoms. E. huxleyi, it is true, is a little smaller, 7.5 /-Lm, than other coccolithophores, 10-22 /-Lm(Hulburt, 1970); but the diatoms, especially the chain-formers,
cover a great range in size. Further, several copepods, particularly the copepodites,
graze down to 5 /-Lmfairly well (Nival and Nival, 1976; Hargrave and Geen, 1970;
Poulet, 1974), and tintinnids graze to 2 /-Lm(Heinbokel, 1978a; b; Spittler, 1973).
Besides, if coccolithophores other than E. huxleyi got less numerous than E.
huxleyi plus diatoms, grazers would then be expected to concentrate their grazing
on the more abundant E. huxleyi-plus-diatom cells or on the larger diatom chains,
because this is what happens experimentally (Poulet, 1973; 1974; 1978; Cowles,
1979; Wilson, 1973; PaffenhOfer and Knowles, 1978; Mullin, 1963).
To say that nutrients differentially produce E. huxleyi, G. oceanica, and diatoms
in greater amounts than the remaining coccolithophores is to account for the
increases of the first group but not to account for the decreases of the second
group in shallow waters as compared to deep water. Therefore, to account for
such decreases stranding is required.
The r-Selected Species Emiliania huxleyi and Gephyrocapsa oceanica
Nutrients should differentially produce greater amounts of E. huxleyi and G.
oceanica than of Cyclococcolithus leptoporus and Thoracosphaera heimii, these
last two occurring in Tables 1 and 2. The reason for this supposition is that
experimentally (Brand and Guillard, 1981) E. huxleyi and G. oceanica have a
maximum growth rate of 2 div/day and C. leptoporus and T. heimii have a
maximum growth rate of 1 div/day. So, if growth conditions are adequate, then
the first pair dominates and the second pair does not dominate. This hypothesis
is partially confirmed by E. huxleyi at 36°N, 66°W and between Bermuda and
Florida but is not confirmed in the Mediterranean, Table 4. (Table 4 shows that
E. huxleyi is more abundant in the first two cases than the sum of all other
coccolithophores, which would certainly make it more abundant than C. leptoporus and T. heimii.)
The case of the Mediterranean, wherein other coccolithophores as a whole
completely overshadow E. huxleyi, indicates that reliance on the greater growth
capacity of E. huxleyi to forecast its dominance bogs down. Then where is G.
208
BULLETIN OF MARINE SCIENCE, VOL. 33, NO.2,
1983
oceanica? It should (but doesn't) dominate in all these situations alongside E.
huxleyi-in fact no G, oceanica were observed in the Mediterranean and BermudaFlorida samples and only 5 cells at 36°N, 66°W. But off Colombia and in the Gulf
of Persia both are abundant, seeming to promote the hypothesis that if growth
conditions are improved, then the two r-selected fast-growers both dominate.
However, this hypothesis partially bogs down too, because in the North Pacific
E. huxleyi solely dominates, the two split dominance about the equator, G. oceanica solely dominates westward in the Gulf of Carpenteria, the Timor and Java
Seas, and the South China Sea, and then the two split dominance again in the
Red Sea (Okada and Honjo, 1973; 1975). Thus finally, a modest hypothesis would
seem to be that if growth conditions are adequate or improved, then one or the
other or both dominate (with the Mediterranean the only disconfirming case).
K-Selection and Quasi-K-Selection
As has been mentioned, Table 4 shows Emiliania huxleyi unabundant, 16 cells/
liter, in the Mediterranean and fairly abundant, 682-1,931 cells/liter, in the Atlantic. But the rest of the coccolithophores are equally abundant from Mediterranean to Atlantic, the total range being 378 to 601 cells/liter. So, if E. huxleyi
is more abundant, then it does not make the other coccolithophores less abundant.
This is to say that E. huxleyi does not force other coccolithophores to change in
concentration by competing with them for nutrients. And analogously, other
species do not force each other, it would seem, to change in concentration by
competing for nutrients. They just share nutrients.
The ordered ranking in Tables I and 2 says, for sure, that coccolithophore
species share nutrients. This is to say that a nutrient concentration 'x' produces
each species concentration 'y' in Table 1 or Table 2. Substituting 'select' for
'produce' we get nutrient 'x' selects species 'y' -or, 'y' is selected by 'x'. More
persuasively we may note that nutrient in low concentration (Menzel and Ryther,
1960) selects the coccolithophore species of Table I and that nutrient in large
concentrations selects the many and abundant diatoms found in upwellings (Hulburt, 1976). If nutrient can be so clearly selective in this way, the issue may be
extended to nutrient's selecting each one of the species of Tables I and 2. This
happens under equilibrium conditions of the Atlantic and Mediterranean sampling-equilibrium
as compared to the non-equilibrium of the Colombia-Ecuador
sampling. Thus there is no problem in the use ofthe transitive verb 'select', either
in the active voice 'x selects y' or passive voice 'y is selected by x.'
When a solid substrate is introduced for organisms to occur on, competition
for space is unavoidable. Whether one notes the competitively shifting proportions
of two mussel species in clumps of mussels on pilings (Harger, 1971-1972), or
of mussel and sea palm on exposed rocky promontories (Paine, 1979), or of species
of incrusting bryozoa on coral undersurfaces and on Fucus (Jackson, 1979; Stebbing, 1973), or of barrier reef corals (Connell, 1973), or of clover and grasses in
a meadow (Turkington and Harper, 1979), or of plant species on badger disturbances in a prairie (Platt, 1975), one is permitted an elliptical use of 'select' to
report one) findings. The better adapted genotype within each species or across
species in a pair or group of species is selected; 'y' is selected over yesterday's
competitors, which are non-existent today, whether yesterday is the brief fortuitousness of several years or the prolonged winnowing process of evolutionary
time. In these spatially competitive but competitively balanced situations there
is no need for mentioning a food resource 'x' as a selector in 'y is selected by x.'
Provided that environmental disturbances or predator-mediated changes are not
HULBURT:
COCCOLlTHOPHORID
PLANKTON
209
such as to open up large portions of substrate to rampant opportunists, we can
view these situations as tending toward true K-selection. Of course, this is only
part of the large overview provided by the 'r-selected, K-selected continuum'
(Southwood, 1976). But the concern here is the peculiar dangling use of the
transitive verb 'select' in 'y is selected.' In the coccolithophore plankton, by
contrast, there is no difficulty in supplying a resource 'x' to correct this dangling
usage; thus 'y' is selected by 'x', yielding quasi-K-selected species.
From the point of view of the evolution of immobile forms, competition is
primarily an accident contingent upon the occurrence of solid substrates, except,
obviously, in deserts where the amount of spatial separation between plants is
dependent on water supply (Woodell et a1., 1969). Where no solid substrates
occur, as in the plankton, and spatial separation between individual organisms is
vast (relative to their size), there is not a clear case for competition, as on the
shore or dry land. But there is a clear case for selection, wherein 'y' is selected by
'x', to provide for quasi-K-selection.
ACKNOWLEDGMENT
The author is indebted to P. Brewer for use of temperature data in the Gulf of Persia.
Contribution No. 5183 from Woods Hole Oceanographic Institution.
LITERATURE
CITED
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119-132.
Brewer, P. G., A. P. Fleer, S. Kadar, D. K. Shafer and C. L. Smith. 1978. Chemical oceanographic
data from the Persian Gulf and Gulf of Oman. Woods Hole Oceanographic Institution Report
78-37.
Connell, J. H. 1973. Population ecology of reef building corals. Pages 205-245 in D. A. Jones and
R. Endean, eds. Biology and geology of coral reefs, v. 2, Biology I. Academic Press, New York
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Cowles, T. J. 1979. The feeding response of copepods from the Peru upwelling system: food size
selection. J. Mar. Res. 37: 601-622.
Emery, K. O. 1956. Sediments and water of Persian Gulf. Bull. Am. Assoc. Pet. Geol. 40: 23542383.
Guillard, R. L. and P. Kilham. 1977. The ecology of marine planktonic diatoms. Pages 372-469 in
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Harger, J. R. 1971-1972. Competitive coexistence: maintenance of interacting associations of the
sea mussels Mytilus edu/is and Mytilus calijornianus. Veliger 14: 387-410.
Hargrave, B. T. and G. H. Geen. 1970. Effects of cope pods grazing on two natural phytoplankton
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-and --.
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--.
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Hentschel, E. 1936. Allgemeine Biologie des Sudat]antischen Ozeans. Wiss. Erg. Deut. Atl. Exp.
Meteor 1925-1927 II: 1-344.
Hulburt, E. M. 1968. Phytoplankton observations in the western Caribbean Sea. Bu]1. Mar. Sci. 18:
388-399.
--.
1970. Competition for nutrients by marine phytoplankton in oceanic, coastal, and estuarine
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BULLETIN OF MARINE SCIENCE, VOL. 33, NO.2,
1983
1976. Limitation of phytoplankton species in the ocean off western Africa. Limnol. Oceanogr.
21: 193-211.
---.
1979. An asymmetric formulation of the distribution characteristics of phytoplankton species:
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--.
1969. Phytoplankton distribution off the North Carolina coast. Am. Mid. Nat. 82: 241-257.
---.
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---.
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--and ---.
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Poulet, S. A. 1973. Grazing of Pseudocalanus minutus on naturally occurring particulate matter.
Limnol. Oceanogr. 18: 564-573.
--.
1974. Seasonal grazing of Pseudocalanus minutus on particles. Mar. BioI. 25: 109-123.
---.
1978. Comparison between five coexisting species of marine copepods feeding on naturally
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HULBURT:
COCCOLITHOPHORID
PLANKTON
211
Wilson, O. S. 1973. Food size selection among copepods. Ecology 57: 909-914.
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OATEACCEPTED: June 23, 1982.
ADDRESS: Woods Hole Oceanographic Institution,
Woods Hole. Massachusetts 02543.
ApPENDIX
Truth value analysis of expressions (4) and (5) is provided as follows, following the method of Quine
(1972).
[Ox :J (Ex. Ox)] :J [(-Ex
Ox :J. Ex. Ox ::J: -Ex
T :J. Ex . Ox ::J: -Ex
V -OX.:J
Ex. Ox .:J -(-Ex
1
V -Ox) :J -Ox]
V -Ox.:J
-Ox
1 :J. Ex . Ox ::J: -Ex V -Ox.:J
V -Ox)
T
T :J T
Ex. Ox .:J. Ex . Ox
T
T
-Ex
V -Ox.:J
-Ox ::J: Dx :J. Ex . Ox
1 V -Ox.:J
-Ox ::J: Dx :J. T . Ox
-Ox:J
-Dx .:J. Dx :J Ox
1:J -Dx .:J. Dx :J T
T:J -Ox .:J. Dx :J 1
T:JT
T
-Dx:J-Ox
T V -Ox.:J
-Dx ::J: Dx :J.1.
T:J -Ox .:J. Dx :J 1
-Dx:J
-Ox
Ox
T
T
Expression (4) is repeated in step 1 of the truth value analysis. Step 2 repeats
step I, putting double dots for brackets and single dots after and before':)' for
parentheses. Thus dots are used for punctuation of parentheses and brackets as
well as for indicating 'and'.
The method of truth value analysis is shown by step 3. One clause, 'Dx', is
given the value truth, '1', to the left and then given the value falsity, '1', to the
right. Where '-Dx' occurs the value '1' for 'Dx' becomes '1'-for the denial of
truth is falsity. Where '-Dx' occurs with 'Dx' as '1' the value of'-Dx'
becomes
'1'-for the denial of falsity is truth.
Steps 4 to 6 at the left and 4 to 5 at the right resolve step 3 to truth for both
the options in step 3. At the left '1' of'T :). Ex. Ox' is dropped because the whole
is true when the consequent 'Ex. Ox' is interpreted as true and is false when the
consequent is interpreted as false. So, all that is needed is the consequent. The
other half of the left part of step 3 is '- Ex v -Ox .:) 1'. The antecedent '- Ex
v -Ox' when interpreted as true would give 'T :) l' for the whole and this
combination is rated as '1'. Then to get this result, just deny a true antecedent:
thus '-(-Ex
v -Ox)'. But when the antecedent is interpreted as false giving
'1 :) 1', this combination is rated as true. So to get this result, just deny a false
antecedent: thus again '-(-Ex
v -Ox)'. So both options of '- Ex v -Ox .:) l'
with true or false antecedent are gotten by just denying the antecedent. The denial
of'Ex' or 'Ox' denied in step 4 isjust both 'Ex' and 'Ox' affirmed, in the consequent
of step 5. Step 5 has both left and right parts the same; so if one is true, so is the
other, and likewise if one is false, so is the other: 'T :) 1', '1 :) 1'. Both of these
are rated as true, step 6, because neither is the flat denial, 'T :) 1', of'T :) 1'.
212
BULLETIN OF MARINE SCIENCE, VOL. 33, NO.2,
At the right in step 3 the value
'1'
1983
assigned to 'Dx' provides for truth of
'1 ::> • Ex . Ox', since it does not matter whether the consequent 'Ex. Ox' is true
or false-one can never get the false combination 'T ::> 1'. When the value '1' is
assigned to 'Dx' in the terminal '-Dx', one gets '1'; and this value, regardless of
the value of the antecedent '-Ex v -Ox', can never yield the false combination
'T ::> 1'.
The bracketed parts of step I are' A' and 'B'. So step I is 'A ::> B', and this
plus its reverse are part of equivalence. Step 7 is 'B ::> A' and truth value analysis
yields final results of truth only. Step 8 shows alternate values given to 'Ex' in
the initial '-Ex'. At the far left the part '1 v -Ox' is true or false depending upon
whether the residual portion '-Ox' is true or false; so '1' is dropped in step 9. To
the right the part 'T v -Ox' is true because just one portion of an 'or-connected'
expression being true makes the whole true. SO 'T v -Ox' resolves to '1' in step
9. The opposite relation obtains in an 'and-connected' expression, as in '1 . Ex'
in step 8, where the '1' spoils the truth of the whole, yielding '1' in step 9. In
'T . Ox' to the left in step 8 'T' may be deleted because both parts of an 'andconnected' statement must be true for the whole to be true, and thus the whole
is true or false according as 'Ox' is true or false. Steps 10-12 follow the conventions
and rules already taken up.
Everywhere the outcome of this exhaustive analysis is truth. So this is part of
equivalence. Equivalence is truth by truth value analysis of both parts of' A ::> B
and B ::> A'. And if both parts of an 'and-connected' statement are true, the whole
is true. So then we say 'A' and 'B' are equivalent under these circumstances.