Download Predicted and Observed Feeding Rates of the Spinose Planktonic

BULLETIN Of MARINE SCIENCE, 35(1): 1-10, 1984
PREDICTED AND OBSERVED FEEDING RATES OF THE
SPINOSE PLANKTONIC FORAMINIFER
GLOBIGERINOIDES SACCULIFER
David A. Caron and Allan W H. Be
ABSTRACT
Planktonic foraminifera feed by using a sticky rhizopodial network to ensnare motile prey.
Rates of capture of zooplankton prey were estimated from the frequency of prey items
observed in the rhizopodia of SCUBA-collected specimens of the planktonic foraminifer
Globigerinoides sacculifer (Brady). Copepods were the dominant prey observed, constituting
44% of the foraminiferal prey numerically, and 95% of the biomass. A simple model was
derived to describe the natural rates of predation by G. sacculifer on zooplankton, based on
non-selective capture of appropriate-sized prey. The model was applied to predict feeding
rates of G. sacculifer on copepod assemblages over a range of values. The model predicted
a wide variability (two orders of magnitude) in the rate of capture of copepods for the range
of variables chosen. Feeding rates estimated from the frequency of cope pods in the rhizopodia
of SCUBA-collected foraminifera also showed a wide variability, averaging one copepod
captured every 3.3 days, and were generally within the range of feeding rates predicted by
the model.
Research on the biology of planktonic foraminifera has not kept pace with
paleontological studies of their shell remains. This apparent lag on the part of
plankton biologists can be attributed largely to an inability in the past to obtain
individuals in good physiological condition for laboratory experimentation, and
to maintain that condition in culture. Ironically, it has been this fastidiousness
to changes in environmental conditions which explains their suitability for the
identification of water masses and climatic variations. As a result, however, our
knowledge concerning the ecological significance of this taxonomic group in plankton ecosystems remains sketchy.
Present collection techniques now allow the rearing of several species of plank-
tonic foraminifera in the laboratory in apparently good health, as evidenced by
a high frequency of gametogenesis (Be and Anderson, 1976; Be et al., 1977;
Spindler et a1., 1978; Be et a1., 1981; Caron et a1., 1982). These studies, as well
as light and electron microscopical examination of freshly-collected individuals
(Anderson et a1., 1979), have shown that zooplankton is a conspicuous component
of the diet of planktonic foraminifera, in contrast to earlier reports which suggested
that they are primarily microherbivores (Lipps and Valentine, 1970). Approximately one-half of the species of planktonic foraminifera have been examined to
date (Anderson et al., 1979), and all show evidence of a carnivorous mode of
nutrition. At least one species, Hastigerina pelagica (d'Orbigny), is exclusively
carnivorous (Anderson and Be, 1976a). In addition, several species of planktonic
foraminifera have now been reared successfully in the laboratory on a carnivorous
diet of Artemia nauplii (Be et a1., 1977).
While yielding valuable information concerning the significance of zooplankton
in the diets of these protozoa, laboratory experiments give little insight into the
natural feeding rates of planktonic foraminifera on zooplankton species in the
ocean. Be et al. (1981) and Caron et a1. (1982) have shown that Globigerinoides
sacculifer (Brady) is capable of survival and growth in laboratory culture over a
wide range offeeding regimes, using Artemia nauplii as food. Due to this flexibility
2
BULLETIN OF MARINE SCIENCE, VOL. 35, NO. I, 1984
Table I. Taxonomic groupings of 191 prey items observed in the pseudopodial network of 1,124
SCUBA-collected G. sacculifer
Prey
Copepoda
Ostracoda
Chaetognatha
Pteropoda
Appendicularia
Siphonophora
Salpae-Doliolidae
Ciliata (tintinnids)
Ciliata (non-tintinnid)
Radiolaria! Acantharia
Miscellaneous
(eggs, polychaete &
decapod larvae)
Unidentified
Size Range
Number
of Prey
(mm)
Observed in
Pseudopodia
% of
Total
0.1-1.5
0.2
1.5
0.2-0.7
2.0-4.0
2.0-4.0
1.G-3.0
0.1-0.2
0.1-0.2
0.1-0.3
0.2-4.0
84
2
9
2
3
45
6
13
4
44.0
0.5
0.5
1.0
4.7
1.0
1.6
23.6
3.1
6.8
2.1
0.1-1.0
21
11.0
I
I
Biomass
(pg C)
59.3
0.1
0.5
0.4
0.7
0.3
1.0
0.2
0.1
0.1
% of
Total
94.9
0.2
0.8
0.6
l.l
0.5
1.6
0.3
in their requirements for particulate food, it is difficult to estimate natural rates
of capture of zooplankton from laboratory experiments. However, estimation of
natural feeding rates is essential for modeling the role which foraminifera play in
plankton communities. These rates determine the magnitude of foraminiferal
grazing effects on zooplankton assemblages, and thus energy flow through this
component of the plankton. Feeding frequency also influences the growth rates
of the foraminifera (Be et aI., 1981; Caron et aI., 1982).
The use of SCUBA for collecting planktonic foraminifera affords a unique
opportunity to investigate these rates. By obtaining individuals of G. sacculifer
in separate jars and examining them for prey organisms entangled in their spines
and rhizopodia, it was possible to determine the type and number of zooplankton
captured. These data were then used to estimate the rate of capture of zooplankton
prey by G. sacculifer using a digestion rate measured in the laboratory. A simple
model was derived which predicts the capture of zooplankton species by G. sacculifer, based on a stochastic collision model. The model was then used to predict
the feeding rates of G. sacculifer on copepod assemblages and these predicted
rates were compared with feeding rates based on the occurrence of copepod prey
in the rhizopodia of SCUBA-collected individuals.
MATERIALS AND METHODS
A total of 1,124 individuals of G. sacculifer were SCUBA-collected approximately 3 km west of
Holetown, Barbados (13·IO'N, 50°31 'W) from October 1978 to April 1979. This species is present
throughout the year off Barbados, and is relatively amenable to rearing (Be et aI., 1981; Caron et aI.,
1982), thus facilitating research on this species.
Collecting procedures have been described previously (Be et aI., 1977). Planktonic foraminifera with
shell diameters of 150-600 ILm were collected routinely. Larger individuals were generally not present
in surface waters, while smaller individuals were not conspicuous to SCUBA divers. Living foraminifera brought to the laboratory at Bellairs Research Institute were identified to species using a Wild
M5 stereomicroscope and a Nikon inverted microscope (model MS). All G. sacculifer individuals
were examined for the presence of zooplankton in the rhizopodia within 2-3 h of collection. A smaller
number of foraminifera were preserved in formalin on the boat to examine the possibility of rapid
digestion of fragile gelatinous zooplankton between time of sampling and examination. The results
for preserved specimens were comparable to those for live individuals. Prey items were identified to
major taxonomic group (Table I), and volume estimates of the prey were made based on their
CARON AND BE: NATURAL FEEDING RATES OF PLANKTONIC
FORAMINIFERA
3
dimensions. For crustacean prey, only exoskeletons which still contained tissue were counted, since
empty exoskeletons may be retained in the rhizopodia for several hours. Volume estimates were
converted to carbon estimates in Table I by assuming that 1 cm' = I g wet weight, dry weight =
0.20 x wet weight, and carbon = 0.40 x dry weight (Beers et aI., 1975). The total number of G.
sacculifer and number of G. sacculifer with prey items were recorded for each collecting trip.
RESULTS
Prey Capture by Globigerinoides sacculifer
G. sacculifer is a widely distributed warm-water planktonic foraminifer (Be and
Tolderlund, 1971). The multi-chambered shell attains a maximum length of approximately 1.1 mm, but the presence of numerous, slender, radiating spines
functionally increases the diameter to 4 mm or more. The spines are used to
support a complex "spider web"-like rhizopodial network which serves the dual
purpose of prey capture and dispersal of symbiotic algae outside the shell (Anderson and Be, 1976b).
The capture of food organisms by G. sacculifer (and all other planktonic foraminifera) is essentially a passive process. Planktonic foraminifera do not actively
pursue prey and are basically stationary with respect to the water mass, although
diel vertical migrations cannot be ruled out (Be, 1960). Prey capture takes place
when food organisms come into contact with the rhizopodial network of a foraminifer. Movement of the zooplankter to extricate itself leads to entanglement
and eventual immobilization. The prey is then drawn close to the shell and
digested. Our observations show that copepod prey (individuals 200-700 .urn in
length) are drawn close to the shell from the distal parts of the spines in 10-15
minutes, at a pulling rate of approximately 100 ",m/min. The copepod body cavity
is subsequently invaded by rhizopodia and the crustacean tissue is transported to
the foraminiferal shell interior (Anderson and Be, 1976a). Digestion of such copepods occurs in 5-6 h, resulting in an empty carapace.
Zooplankton Prey of SCUBA-Collected G. sacculifer
The occurrence of a diverse array of zooplankton in the rhizopodia of G.
sacculifer suggests that species selectivity is not a crucial factor in prey acceptability
(Figs. 1-6; Table 1). Appropriate size and vigor appear to be the major criteria
for prey capture. The maximum size of a zooplankter which can be captured is
dependent on its morphology (which provides a surface for rhizopodial attachment), swimming speed, and vigor. Relatively few strong swimmers (e.g., chaetognaths, pteropods) were observed as prey in the rhizopodia (Table 1), suggesting
that large specimens of these taxa are normally not captured. An upper limit for
copepods appeared to be about 1.5 mm in total body length, based on occurrence
in SCUBA-collected foraminifera. These results are also supported by our (unpublished) observations made on foraminifera offered freshly-collected zooplankton in the laboratory.
Copepods were the dominant prey, accounting for 44% of all organisms observed, but a large variety of other organisms were captured and digested. The
wide range of prey that G. sacculifer accepts may be an adaptation to cope with
the relative scarcity of prey in oligotrophic oceanic plankton communities. In this
respect G. saccullfer is unlike some ben.thic foraminifera which show specificity
in food selection (Lee et aL, 1966). The predominance of copepods as prey items
for a non-selective predator is consistent with zooplankton distribution studies
off Barbados, which have shown that copepods are the numerically dominant
group (Greze and Bileva, 1979; Lewis and Fish, 1969; Moore and Sander, 1977).
4
BULLETIN OF MARINE SCIENCE, VOL. 35, NO. I, 1984
CARON AND BE: NATURAL FEEDING RATES OF PLANKTONIC
FORAMINIFERA
5
They comprised an average of 88% of the motile zooplankton over a 28-month
sampling period (Moore and Sander, 1977). Estimates of the biomass represented
by the various taxa (Table 1) indicate that copepods were by far the dominant
component of the diet, comprising approximately 95% of the carbon obtained
from zooplankton. Tintinnid ciliates were also common prey (presumably due to
their abundance, rapid swimming speed, and suitable size), but due to their small
cell biomass contributed little to the total diet. While Appendicularia and Radiolaria/ Acantharia are also abundant in the plankton (second and third numerically behind copepods; Greze and Bileva, 1979) they occurred infrequently in
the rhizopodia, presumably due to their relatively low mobility.
Although a wide taxonomic range of zooplankters were observed within the
rhizopodia and spines of G. sacculzfer, we have noted that some types of organisms
were ensnared but were subsequently rejected. The rejected zooplankters include
some siphonophores, echinoderms and sipunculid larvae, larcoidean radiolaria,
and polychaetes, some of which may either secrete or possess noxious chemicals
or hard structures that render them "unpalatable" to G. sacculifer.
The Model
Due to the apparent non-selective nature of prey capture for G. sacculifer, a
simple stochastic collision model describing predation as the chance encounter
between a motile zooplankter and a foraminifer can be derived readily if several
simplifying assumptions are made: (1) Foraminifera and zooplankton prey are
represented as spheres, and contact by collision results in capture of the zooplankter by the foraminifer. The radius of these spheres is defined as the encounter
radius. An analogous representation has been employed for motile predatory
zooplankton, where the encounter radius was determined by the predator's sensory
system (Feigenbaum and Reeve, 1977; Gerritson and Strickler, 1977; Giguere et
al., 1982); (2) Zooplankton are randomly distributed and move randomly in the
water at some average velocity, while the foraminifera are stationary with respect
to the water mass; (3) Prey density is constant; (4) Foraminifera feed continuously,
and feeding rates are the same throughout the day; and (5) All encounters between
zooplankters and foraminifera lead to the capture of the zooplankter (i.e., all
appropriate organisms encountered are eaten, and capture efficiency = 100%). It
also is assumed in the derivation that the contribution of phytoplankton food is
negligible relative to the zooplankton contribution. A discussion of the validity
of these assumptions will be given later.
Consider a zooplankter with encounter radius Rp moving randomly through a
volume of water at some average velocity, v. Foraminifera with encounter radius
Rf are also distributed randomly in the water. The zooplankter moves safely
through the water (i.e., no encounters with foraminifera) as long as the distance
from the center of the zooplankter to the center of any foraminifer is always
greater than Rf + Rp. However, if at any time the distance from center to center
is less than or equal to Rf + Rp, contact between foraminifer and zooplankter is
made, and the zooplankter is entangled and captured. Therefore, with respect to
zooplankter-foraminifer encounters, the zooplankter sweeps out a volume per
unit time along its axis of movement as described by the following equation:
Figures 1-6. Diverse natural prey organisms of Globigerinoides sacculifer. (I) copepod (75 x), (2)
appendicularian (75 x), (3) pteropod (30 x), (4) acantharian (75 x), (5) chaetognath (30 x) and (6) fish
larva (30 x).
6
BULLETIN OF MARINE SCIENCE, VOL. 35, NO. I, 1984
Volume/time
= (v)(rr)(Rr + Rp)2
(1)
Consider, now, a number of different-sized zooplankters in several different
taxa moving about a stationary foraminifer with velocities unique for each taxon.
If there are N taxa present, each with ni individuals per unit volume, it follows
that the number of encounters the foraminifer will experience is given by the
equation:
i=J
No. of Encounters/time
= (rr) ~ (vJ(nJ(Rr + RpY
(2)
N
where Vi is the average swimming speed, Rp; is the encounter radius, and nj is the
number of individuals per unit volume for zooplankters in the ith taxon, respectively.
The application of equation 2 for the prediction of feeding rates of G. sacculifer
requires much more information than is presently available for any single prey
species, let alone the wide array of prey organisms observed in the rhizopodia of
the SCUBA-collected specimens. However, given that copepods constitute the
major food source for G. saccuhfer (Table 1), it is possible to obtain a rough
estimate of the natural feeding rates of G. sacculifer for copepods only. Equation
2 then becomes:
No. of Encounters/time
= (n)(v)(rr)(Rr
+ Rp)2
(3)
where n is the average density of copepods of appropriate size, v is their average
swimming speed, and Rp is their average encounter radius.
A range of encounter rates between a G. sacculifer individual and a copepod
assemblage was calculated from equation 3. This range encompasses the lower
and upper limits of encounter rates which can be expected for G. sacculifer. based
on the assumptions discussed below. Encounter radius of the foraminifer (Rr =
1.5 mm) was based on the size commonly observed in SCUBA-collected individuals. Spine length was remarkably constant (I300!-tm ± 50 !-tm) for shell lengths
between 175 and 575 !-tm. Encounter radius of the copepods (Rp) was based on
the maximum size of copepods observed in the rhizopodia of SCUBA-collected
G. sacculifer (1.5 mm) and the length of copepod nauplii (-0.2 mm). Swimming
speeds (v) of 1-5 mm/sec were based on Hardy and Bainbridge (1954) and Purcell
(1981). Copepod density (n) was based on Moore and Sander (1977), who reported
an average of 135 copepods/m3 off Barbados over a 28-month sampling period.
However, only a portion of these individuals are of acceptable size. Since information concerning the size distribution of copepods was unavailable, a range of
10-100 copepods/m3 was used for predicting feeding rates in this study.
The encounter rates predicted from equation 3 between a G. sacculifer and
copepod prey varied from a minimum ofO.007/day (1 copepod every 145 days)
to a maximum ofO.687/day (1 copepod every 1.5 days) for the values chosen for
the variables. We believe that the variability in encounter rates predicted from
equation 3 has real implications for foraminiferal feeding frequency, and may be
one explanation for the wide tolerances in particulate food requirements observed
for G. sacculifer (Be et aI., 1981; Caron et aI., 1982). Those studies indicated that
feeding Artemia nauplii to foraminifera at the rate of one nauplius per day or one
every 7 days resulted in no significant differences in the number of individuals
which eventually reached reproductive maturity.
The frequency of occurrence of prey in the rhizopodia of SCUBA-collected G.
sacculifer is given in Table 2. These frequencies were used to calculate encounter
rates between foraminifera and copepod prey using an average digestion rate of
CARON AND BE: NATURAL
FEEDING RATES OF PLANKTONIC
7
FORAMINIFERA
Table 2. Frequency of occurrence of copepods in the rhizopodial networks of 1,124 SCUBA-collected
G. sacculifer on 23 sampling dates (The calculated rates of encounter between copepods and foraminifera are based on a 6 h digestion time for the copepods)
Number orG.
Collection Date
19 Oct
25 Oct
14 Nov
27 Nov
4 Dec
8 Jan
16 Jan
24 Jan
29 Jan
13 Feb
20 Feb
21 Feb
26 Feb
2 Mar
13 Mar
27 Mar
3 Apr
5 Apr
9 Apr
10Apr
18 Apr
20 Apr
23 Apr
1978
1978
1978
1978
1978
1979
1979
1979
1979
1979
1979
1979
1979
1979
1979
1979
1979
1979
1979
1979
1979
1979
1979
Foraminifera
with
saccuilfer
Copepod Prey
Observed
(%)
(encounters/day)
54
67
32
90
92
24
78
59
46
51
69
48
5
15
25
22
31
20
80
30
75
62
49
5.6
13.4
0.0
3.3
5.4
4.2
3.8
3.4
15.2
2.0
11.6
8.3
20.0
0.0
4.0
4.5
6.5
10.0
10.0
10.0
9.3
14.5
8.2
0.22
0.54
0.00
0.13
0.22
0.17
0.15
0.14
0.61
0.08
0.46
0.33
0.80
0.00
0.16
0.18
0.26
0.40
0.40
0.40
0.37
0.58
0.33
1,124
x = 7.5
x = 0.30
Encounter
Rate
6 h. Observed encounter rates were highly variable. The percentage of specimens
with copepod prey varied from 0 to 20%, with a mean of7.5%. These frequencies
represent encounter rates of 0 to 0.80/day (1 encounter every 1.3 days), with a
mean of 0.30/day (l encounter every 3.3 days). One specimen contained two
copepods (treated in Table 2 as 2 encounters). The between-sample variability in
the occurrence of prey in the rhizopodia of G. sacculifer probably reflects the large
short-term oscillations in copepod abundance off Barbados (Sander and Moore,
1978) and mirrors the large variability in encounter rate predicted by the model.
The rate of digestion of zooplankton prey by G. sacculifer is dependent on the
nutritional status ofthe foraminifer. A digestion time of 6 h represents an average
based on laboratory observation of G. sacculifer offered net-collected copepods.
If digestion times of 3 hand 8 h (roughly the range observed) are applied to the
data in Table 2, average encounter rates of 0.23/day (1 copepod every 4.4 days)
and 0.60/day (1 copepod every 1.7 days), respectively, are obtained.
DISCUSSION
Although a carnivorous mode of nutrition was described for planktonic foraminifera over 70 years ago (Rhumbler, 1911), only recently has the extent of this
mode of nutrition become evident (Anderson et aI., 1979). This oversight can
probably be attributed to inappropriate sampling techniques (the spines of foraminifera are damaged during plankton-net collection) and the preponderance of
information on benthic species which apparently consume more algal prey (see
8
BULLETIN OF MARINE SCIENCE, VOL. 35, NO. I, 1984
review by Lee, 1980). The relative importance of zooplankton and phytoplankton
to the diet of planktonic foraminifera still remains largely unknown. While the
capture of algae would be expected to be more frequent due to their greater
abundance, the biomass of a single zooplankter is many times that of individual
phytoplankton prey. The absence ofa simple means to measure the digestion rate
of phytoplankton prey obviates the use of prey frequency data (as in Table 2) in
deciphering the relative importance of these two types of prey.
Another question concerning the nutrition of planktonic foraminifera is the
contribution which symbiotic algae make to the diet of their host. G. sacculifer
possesses dinoflagellate symbionts (Anderson and Be, 1976b). While these symbionts may affect shell growth of the host (Be et aI., 1982) and may contribute
significantly to meeting the energy demands associated with gametogenesis (Be et
aI., 1983), Caron et al. (1982) have shown that food assimilated from the symbionts, or even digestion of the symbionts are not sufficient to support normal
ontogenetic growth of G. sacculifer.
In the strictest sense, there can be objections to any or all of the assumptions
made in constructing this model. Representation offoraminifera as spheres seems
justified, but this assumption is less applicable for prey due to their irregular
morphology. Zooplankton are not distributed randomly in the water and movement also is not random. Patterns of movement will vary among different prey
taxa. For example, the hop-and-sink movement of copepods differs markedly
from the darting motion of chaetognaths. While this does not necessarily alter
the basic model describing prey motion as an advancing cylinder of radius Rp, it
does complicate description of the path of movement and average velocity. Furthermore, prey density may change due to seasonal or successional effects, predation, or vertical migration.
Foraminifera apparently feed continuously. Our laboratory observations have
shown that adult foramiriifera can accept and digest more than five Artemia nauplii
in a 24-h period. However, since prey densities may vary on a diel cycle, the
frequency of prey in the rhizopodia of G. sacculifer in this study (all daylight
collections) may not be indicative of night time feeding rates. Capture efficiency
(i.e., the number of encounters which result in prey capture) is not known for G.
sacculifer in situ. An efficiency less than 100% would result in lower feeding rates
than predicted by the model. The attraction of prey to the foraminifera, or conversely the avoidance of foraminifera by prey would also result in a deviation
from the expected feeding rate.
While these arguments place many caveats on predictions made by the model
at present, it does provide a first attempt to determine the natural predation rates
of planktonic foraminifera for zooplankton, and a framework for future work.
SCUBA collection provides a unique tool to obtain specimens for the examination
of prey in the foraminiferal rhizopodia. The frequency of prey in the rhizopodia
is a reflection of the rate of capture of zooplankton by foraminifera in situ, and
thus a direct verification of the applicability of the model. Plankton tows taken
concurrently with SCUBA collection of foraminifera can be used to provide a
description of the types and densities of zooplankton available to the foraminifera
at the time of collection. Electivity indices may then be employed to determine
the applicability of a model based on collision theory. In short, the model is a
testable hypothesis.
It has been shown that the rate of growth and reproduction of G. sacculifer is
strongly dependent on the feeding frequency (Be et aI., 1981; Caron et aI., 1982).
Those studies concluded that G. sacculifer in the Barbados region fed at a rate
equivalent to one Artemia nauplius every 4 days. The predation rates for copepods
CARON AND BE: NATURAL
FEEDING RATES OF PLANKTONIC
FORAMINIFERA
9
observed in this study (x = I copepod every 3.3 days; Table 2) are consistent with
rates predicted by Be et al. (1981). Thus, feeding rate models may be useful for
the estimation of turnover times of foraminiferal populations in nature when
interpreted in conjunction with laboratory studies. In addition, information on
the natural rates of feeding by planktonic foraminifera can be used to provide
optimal conditions for laboratory specimens to assure healthy individuals for
experimentation.
A feeding model based on collision theory provides the simplest view of foraminiferal predation. It will undoubtedly become more complicated as more lifehistory information becomes available for planktonic foraminifera. However,
these protozoa may eventually provide a more manageable predator-prey system
to model than most zooplankton-zooplankton interactions, since the relative immobility of one member (foraminifera) should simplify the derivation of a model
describing these interactions.
ACKNOWLEDGMENTS
This work was supported by National Science Foundation grants OCE78-25450 and OCE81-17715
awarded to A. W. H. Be and O. R. Anderson of Lamont-Doherty Geological Observatory. The
assistance of F. Sander, Director, and the personnel at the Bellairs Research Institute, St. James,
Barbados is gratefully acknowledged. We also thank W. Faber Jr. for field assistance, and Drs. O. R.
Anderson, T. J. Cowles and L. P. Madin for helpful comments on the manuscript. This is Woods
Hole Oceanographic Institution Contribution No. 5525 and Lamont-Doherty Geological Observatory
Contribution No. 3539.
It is with sorrow that the senior author acknowledges the death of Dr. Allan W. H. Be on October
13, 1983, following the acceptance of this manuscript for publication. Dr. Be has been a driving force
in the study of planktonic foraminifera. His enthusiastic and creative approach to research has resulted
in significant advancements in our understanding of the general biology and ecology of foraminifera.
His contributions will not be forgotten.
LITERATURE
CITED
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-and --.
1976b. The ultrastructure of a planktonic foraminifer, Globigerinoides sacculifer
(Brady), and its symbiotic dinoflagellates. J. Foram. Res. 6: 1-21.
--,
M. Spindler, A. W. H. Be and C. Hemleben. 1979. Trophic activity of planktonic foraminifera. J. Mar. BioI. Ass. U.K. 59: 791-799.
Be, A. W. H. 1960. Ecology of recent planktonic foraminifera: Part 2. Bathymetric and seasonal
distributions in the Sargasso Sea off Bermuda. Micropaleontology 6: 373-392.
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-and D. S. Tolderlund.
1971. Distribution and ecology of living planktonic foraminifera in
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Riedel, eds. Micropaleontology of oceans, Cambridge Univ. Press, London.
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D. A. Caron and O. R. Anderson. 198!. Effects of feeding frequency on life processes of the
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--,
H. J. Spero and O. R. Anderson. 1982. Effects of symbiont elimination and reinfection on
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DATEACCEPTED: September 12,1983.
ADDRESSES: (D.A.C.) Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, 02543;
(A. W.H.B. deceased) Lamont-Doherty Geological Observatory of Columbia University, Palisades, New
York, 10964.