Journal of Plankton Research Vol.20 no.l pp.121-133, 1998
Heterotrophic protozoa and small metazoa: feeding rates and
prey-consumer interactions
G.-A.Paffenhofer
Skidaway Institute of Oceanography, 10 Ocean Science Circle, Savannah,
GA 31411, USA
Abstract. A common approach to divide zooplankton into groups has been by size or size fractionation (micro-, meso- and macrozooplankton). Whereas almost all zooplankton retained by 200 um
mesh are metazoa, those not retained are proto- and metazoa. Even so, the variability of major taxa
among those retained by 200 (jm mesh can range widely between samples, that of passing 200 urn can
vary even more when considering the grazing impact. If heavily weighted towards protozoa, the
<200 um community feeding rate on small phytoplankton could be several times the rate when most
animals would be metazoa. Also, the interaction between proto- and metazooplankton passing 200 urn
mesh ought to be considered, as should be that among protozoa. Using published data from the North
Atlantic Ocean, the potential impact of small metazooplankton on the chlorophyll standing stock and
primary productivity as well as on protozooplankton was evaluated. It was found that metazooplankton passing <200 um mesh removed a much larger part of the primary productivity than those
retained by 200 um mesh. Although the biomass of the <200 um mesh metazoa was close to that of
protozoa passing the same mesh, their ration was only a relatively small part of the primary productivity ingested by the latter. Yet, due to their unusually high abundance in these oceanic waters, the
overall metazooplankton appeared to come close to controlling protozooplankton >50 um3 in volume,
i.e. those which could be actively perceived. It is hypothesized that in the absence of control by metazooplankton, protozoa control their own abundance by predation/cannibalism.
Introduction
The size distribution of plankton is traditionally defined by being retained by or
passing certain meshes. For example, organisms <2000 um and retained by
200 um mesh are considered as mesozooplankton, and those passing 200 um mesh
as microplankton. Whereas nearly all organisms retained by 200 um mesh are
metazooplankton, those passing it are proto- and metazooplankton. Passing a
mesh is probably due more to the width of an organism than its overall size or
volume. The importance of mesh width has been recently pointed out by Krsinic
and Lucic (1994) and by Miller (1995). The latter examined various observations
on mesh retention versus organism width and concluded that even copepods
wider than the mesh width generally passed it. Not being able to distinguish
between protozoa and small metazoa may result in misinterpretations of the
microplankton's activity, e.g. the impact of this group on primary productivity.
Among the metazoa which have a width of <200 um are nauplii and copepodid
stages of cyclopoid and small calanoid copepods. Of the often abundant copepod
genera such as Paracalanus, Clausocalanus, Oithona, and Oncaea, the majority of
copepodid stages have a cephalothorax width of <200 um, implying that they will
not be retained quantitatively by mesh of that size and therefore should belong
to the microzooplankton. They are known to ingest auto- and heterotrophic cells
(Stoecker and Capuzzo, 1990), many of them being efficient grazers on cells as
narrow as 4-5 um in width or diameter (Paffenhofer, 1984; Berggreen etal., 1988).
© Oxford University Press
121
G.-A.Paffenhofer
This implies that they can ingest not only small phytoplankton but also a wide
range of the protozooplankton.
Information about the contribution of these small metazoa to the removal of
phytoplankton and protozoa in field studies is scarce (Vinogradov et al., 1976;
Verity et al., 1993). The contribution of phytoplankton as food of the larger
metazoa, i.e. the mesozooplankton, in recent oceanic studies was 5% or less of
the daily primary production (Dam et al., 1993, 1995; Miller, 1993). This can be
attributed to (i) the inability of crustacean mesozooplankton to ingest cells near
5 um diameter or smaller in larger quantities, (ii) their inability to respond rapidly
with high growth and reproduction rates when food becomes abundant (Hutchings, 1992), and (iii) insufficient abundance, in many cases, to control phytoplankton growth (Martin, 1970; Peterson et al., 1990). However, there may be
instances when phytoplankton may be controlled by copepods (Smith and Lane,
1988; Nielsen and Ki0rboe, 1994) or tunicates (Paffenhofer and Lee, 1987).
The goal of this study was to address four questions:
(i) What are the consumption rates of the various components of the microzooplankton community?
(ii) At which abundances may metazooplankton control or reduce the abundance of protozooplankton?
(iii) Why can heterotrophic protists eat far more, and therefore grow faster than
copepods?
(iv) Why are ciliates in offshore waters usually limited in abundance, i.e. do not
develop blooms as compared to copepods?
Method
The field data originated from the JGOFS North Atlantic Ocean study during
May of 1989, and from an extended Soviet study in the equatorial Pacific Ocean
(Vinogradov et al., 1976). First, the carbon biomass and abundance of heterotrophs, the ingestion rate of each group, as well as their weight-specific ingestion
rates are presented (Table I, Verity et al., 1993). The study by Verity et al. (1993)
was chosen because it is the only one so far which covers all the microzooplankton variables quantitatively, i.e. the various protozooplankton components, and
nauplii as well as copepodid stages passing 200 um mesh (Table I). Co-occurring
studies by Chipman et al. (1993), Martin et al. (1993), Joint et al. (1993) and
Sieracki et al. (1993) provided data on overall primary productivity and of its components, and of vertical cell size distribution during the chosen study period. All
these variables were required to assess interactions among the various plankton
components thoroughly. Since Morales et al. (1993) indicated high abundances of
calanoid and cyclopoid copepods, it was assumed that half of the nauplii and
copepodid stages belonged to the first and the other half to the latter group. As
ingestion rates for calanoids, we applied those from Paffenhofer (1984) for
Paracalanus sp. which were being offered simultaneously Isochrysis galbana
(average diameter 4.5 urn, concentration 0.1 mm3 = 20 ug C I"1) and Thalassiosira
fluviatilislweissflogii (average diameter 11 um, concentration 0.1 mm3 I"1 = 8 ug
C I"1) at 20°C. The combined food concentration used then (28 ug C I"1) was thus
122
Heterotrophic protozoa and metazoa
in the range of the heterotrophs available to these metazoans (Table 8 of Verity
et al, 1993,16.3-37.9 ug C I"1). The average daily primary productivity >5 urn in
the upper 35 m was estimated as 14.7 ug C nr 3 , representing a combination of
data from Chipman et al. (1993), Martin et al. (1993), and Joint et al. (1993). Cells
>5 urn were chosen because from experimental studies by Paffenhofer (1984) and
Berggreen et al. (1988), it appeared that the lower size which could be actively
perceived by nauplii and early copepodids of small copepods appeared near
4-5 um diameter. The clearance rates employed were for NIV/V and CI/II of
Paracalanus sp. at 20°C, corrected with a Qw of 3.0 (Sabatini and Ki0rboe, 1994)
to 13.5°C. The rates for Oithona sp. (Cyclopoida) were based on results from
Sabatini and Ki0rboe (1994) on Oithona similis. We assumed that the 'average'
Oithona nauplius during May 1989 was NIV weighing -60 ng C, and the average
Oithona copepodid not retained by 200 um mesh was CII of -200 ng C. These
authors indicated that daily metabolic expenditures of Oithona near 15°C ranged
from 10 to 22% of their body carbon. A value of 16% and an assimilation
efficiency of 66% were assumed which implied that 24% of body carbon needed
to be ingested just to cover metabolic expenditures. To have some modest growth,
we assumed that at least 30% of body carbon needed to be ingested. These
assumptions required that 0.8 and 1.3 ml be swept clear daily by an Oithona NIV
and CII, respectively, at the average heterotrophic potential prey concentration
encountered on 20, 25, and 29 May, 1989 by these juveniles (Verity et al., 1993).
These values were not corrected from 15 to 13.5°C. A Paracalanus sp. NIV
cleared on average 0.65 ml day 1 , and a CI/II 5.3 ml day-1 (Paffenhofer, 1984).
Table I. Carbon biomass C (ug C I"1), abundance A (number I"1, only for nauplii and copepodid
stages), community ingestion I (ug C day-' I"1) and weight-specific ingestion Isp (ug C ug-' C day-1) of
as many as five different planktonic taxa (modified from Verity et al., 1993) in the North Atlantic
Ocean
Taxa
20 May, 1989
25 May, 1989
29 May, 1989
Ciliates
C
I
3.4
8.0
2.35
4.8
11.6
2.42
30.4
72.9
2.40
13.0
220
4.7
0.36
13.6
230
4.9
0.36
15.3
260
5.5
0.36
Nauplii
C(ugCH)
1
A (no. I" )
I
\
Copepodid stages
A (no. 1-')
Dinoflagellates
C
I
!
sp
42
76
49
1.5
3.8
2.53
2.3
5.8
2.52
3.2
8.0
2.50
11.4
35.6
3.12
15.5
48.4
3.12
4.3
13.4
3.12
16.3
22.6
37.9
Heterotrophic
microflagellates (>50 um')
C
I
All protozoa
C
123
G.-A.Paffenhofer
Results
Abundance of micrometazooplankton
This analysis includes 3 of the 6 days covered by Verity et al. (1993): 20, 25, and
29 May, 1989. The biomass of nauplii surpasses that of early copepodids on 2 of
the 3 days (Table II). The overall biomass of nauplii and early copepodids is in
excess of that of the night-time mesozooplankton collected during the same
period which ranged from 14.0 to 19.0 mg C m~3 (Dam et al., 1993). The concentration of nauplii and copepodid stages was unusually high during late May 1989
(Table II) and resembled those found in inshore or nearshore waters rather than
those found in the open ocean (Fulton, 1984). These high concentrations
appeared to have been the result of a sudden burst of reproduction and low
predation. High concentrations of small copepods were also found by Morales et
al. (1993) who observed 8000 Clausocalanus sp n r 3 and 7000 Oithona sp m~3 in
the North Atlantic in spring of 1990, despite using a net of 200 um mesh which
does not retain these genera quantitatively.
Feeding on phototrophic cells
The volume swept clear (VSC) by the nauplius community varied little between
the three dates, whereas that by the early copepodids was elevated on 25 May due
Table II. Abundance, and rates of clearance and ingestion of small metazooplankton in the North
Atlantic Ocean during May 1989 (part of the data from Verity et al., 1993, and from Sieracki et al.,
1993)
20 May, 1989
Nauplii
Copepodids
(Total)
Abundance
220
42
(no. 1-')
Biomass
13.2
8.4
(mg C m-3)
(21.6)
166
VSC
159
(lnr'day-1)
(325)
2.34
2.45
I pp
(mg C nr 3 day-')
(4.79)
(14)
*-phyto > 40 tim'
(mg C m"3)
(4.55)
*phyto > 40 jjm'
(mgCm^day-1)
(0.22)
pp *p
(mgCmg-1 Cday-')
4.7
^phyto
(mgCm^day- 1 )
0.36
Isp
25 May, 1989
Nauplii
Copepodids
(Total)
29 May, 1989
Nauplii
Copepodids
(Total)
230
260
76
13.8
49
15.2
(29.0)
167
300
(467)
2.46
4.41
(6.87)
(15)
15.6
9.8
(25.4)
188
190
(378)
2.76
2.80
(5.56)
(15)
(7.01)
(5.67)
(0.24)
(0.22)
4.9
5.5
0.35
0.35
VSC, volume swept clear; I™,, ingestion rate of primary production; Cphyt0, concentration of plastidic
nanoplankton; I phyto > «, vm>, = ingestion rate of plastidic nanoplankton by nauplii and copepodids;
Ipp sp. weight-specific ingestion rate of primary production; Iphyio. ingestion rate of nauplii feeding on
phytoplankton (from Verity et al, 1993, their Table 8); IsP, weight-specific ingestion rate of nauplii
(calculated from Verity et al., 1993).
124
Heterotrophic protozoa and metazoa
to increased abundance (Table II). These early copepod juveniles together cleared
from -32 to 47% of the cells which they could actively perceive (>5 urn diameter).
This implied that these animals removed 4.8-6.9 mg C m~3 of the total primary
productivity daily which amounts to 15-21% of the total average daily productivity
of 32 mg C nr 3 in the upper 35 m (Chipman et al., 1993; Martin et al., 1993).
Ingestion rates of early juveniles (Iphyt0 > 40 Mm3> Table II) on the standing
stock of plastidic nanoplankton >40 um3 cell volume were similar to Ipp (Table
II). The values for plastidic nanoplankton originated from Sieracki et al. (1993)
who presented vertical distributions of plastidic nanoplankton and, separately,
cell size distribution. The weight-specific ingestion rates of these early juveniles
feeding on phototrophs ranged from 22 to 24% of their body weight (Table II).
Comparative values for daily ingestion rates by nauplii (Iphyto) are from Verity et
al. (1993) which were about twice as high as those calculated above (Table II) due
largely to higher algal growth rates in their experiments. The mesozooplankton
(passing 2.0 mm but retained by 0.2 mm mesh) were thought to have removed
1-5% of primary productivity daily during April and May, 1989 (Dam et al., 1993).
According to Verity et al. (1993) the entire microzooplankton (ciliates, dinoflagellates, microflagellates >50 urn3, and nauplii) ingested daily between 37 and
100% of the daily primary production occurring in their experimental jars.
Feeding on heterotrophic cells
The diet of metazooplankton is not limited to autotrophic cells (Stoecker and
Capuzzo, 1990). Early juvenile copepods can ingest even ciliates (Stoecker and
Egloff, 1987). Therefore, we applied the clearance rates used earlier for estimation of grazing on phytoplankton to calculate ingestion rates on ciliates,
heterotrophic dinoflagellates and microflagellates by metazooplankton <200 um
(Table 8 from Verity et al., 1993). These clearance rates should be minimum estimates because (i) all three groups of protists are mobile i.e. provide hydrodynamic signals to Oithona, and {ii) copepodid stages of another open water
calanoid removed a larger percentage of heterotrophs than of autotrophs of the
same or larger size (Verity and Paffenhofer, 1996). Utilizing concentrations of
available heterotrophs (CH) from Verity et al. (1993) the metazoa passing 200 um
mesh removed daily (IH) between 5.3 and 14.3 mg C m~3 (Table III) ranging from
32 to 47% of the heterotroph standing stock. These amounts represented from
25 to 56% of their body carbon (Table III).
Adding the previously estimated ingestion of phytoplankton (Table II) to that
of heterotrophs, the small metazoa ingested 47%, 58%, and 78%, respectively
(Ixsp), of their body carbon on each of these three days (Table III). A larger percentage of their diet originated from heterotrophs than from autotrophs. These
values are not approaching the satiation level of these early stages. Paracalanus
sp. late nauplii reach maximum ingestion rates near to above 100 ug C I"1 of food
(Figure 1). The concentrations of utilizable food encountered here were near
12-14 ug C I"1 of plastidic nanoplankton >5 um diameter (Sieracki et ai, 1993)
and from 16 to 38 fig C I"1 of heterotrophs, therefore reaching total available food
levels from -28 to -52 ug C I"1.
125
G.-A.Paffenhofer
Table BU. Concentration of heterotroph food organisms (from Table I), ingestion rates of these by
small metazooplankton, and total ingestion rates (photo- and heterotrophic food)
20 May, 1989
Nauplii
Copepodids
(Total)
CH
(16.3)
(mg C m-3)
IH
2.60
2.70
(mg C m-1 day-1)
(5.30)
(0.25)
'HSp
(mgCmg- 1 d a y ' )
(10.09)
h
(mgCm-'day- 1 )
%I PP
(47.5)
%I H
(52.5)
(0.47)
lisp
(mg C mg-1 day-')
25 May, 1989
Nauplii
Copepodids
(Total)
29 May, 1989
Nauplii Copepodids
(Total)
(22.6)
3.60
6.48
(10.08)
(0.35)
(37.9)
7.14
7.18
(14.32)
(0.56)
(16.95)
(19.88)
(40.5)
(59.5)
(0.58)
(28.0)
(72.0)
(0.78)
C H , concentration of heterotroph protozoa; I H , ingestion rate of heterotroph protozoa by nauplii and
early copepodids; I H s p . weight-specific ingestion rate on heterotrophs; IT, total ingestion rate by
nauplii and early copepodids (photo- and heterotroph food); Ijs p , weight-specific total ingestion rate.
Discussion
A comparison of the feeding rate calculations of small metazooplankton with that
on feeding of mesozooplankton (Dam et ai, 1993) and protozooplankton indicates that during late May 1989 in the North Atlantic weight-specific feeding rates
had the following sequence:
protozooplankton > micrometazooplankton > mesozooplankton.
In an effort to understand the above sequence and that of interactions among
the proto- and metazooplankton, it will be attempted in the following paragraphs
to evaluate first the significance of these abundant zooplankton groups as consumers; second, under which conditions metazooplankton may control or reduce
ciiiate abundance; and third, why ciliates grow so much faster than copepods and
are usually limited in abundance in offshore waters as compared to copepods.
Significance of copepods and protozooplankton as consumers
Our results show that the biomass of copepods passing 200 um mesh (Table II)
was close to that of protozoa (Table I) and slightly exceeded that of mesozooplankton which were mainly copepods (14-19 mg C nr 3 during dark hours, Dam
et ai, 1993). Therefore, the observed higher removal of phytoplankton by protozoa than copepods may not be so much a function of differences of biomass
because:
(i) Small copepods only retain phytoplankton particles >4-5 um diameter rather
efficiently (efficiency increasing with particle size) and therefore will not impact
cells near or below that size significantly (Paffenhofer, 1984; Berggreen et al,
1988). Nauplii and early copepodids of small copepods will attain near maximum
126
Heterotrophic protozoa and metazoa
oU n
$p
(Paffenhofer 1984)
200-
FOOD: U = UnialSal
M = Multialgal
O • -NaupKusE
• D "CofwpodX
(Dolan& Coats 1991)
•
Euplotes woodruffi
65\mESD
FOOD: Metanophrys
15.6\MESD
20
SO
T
100
150
1
Food Concentration (ngC - I " )
Fig. 1. Weight-specific ingestion rates in relation to utilizable food concentration for the ciliate
Euplotes woodruffi and juveniles of the calanoid copepod Paracalanus sp. Late nauplii and early copepodid stages of Paracalanus sp. had been offered solely the diatom Thalassiosira weissflogii, and as
multialgal food the flagellate Isochrysis galbana, and the diatoms T.weissflogii and Rhizosolenia alata
of which the latter could not be ingested by these juvenile stages and therefore was not included in
the food concentration.
feeding, and growth rates only at food concentrations >100 ug C I"1 (Figure 1),
especially in nature where these copepods will encounter various different types
of food which reduces their ingestion rates as compared to feeding on one type
of food (Figure 1; Paffenhofer, 1984). The presence of heterotrophic cells may
even further limit their impact on phytoplankton (Verity and Paffenhofer, 1996).
(ii) Larger copepods will only perceive particles >10 urn actively (Paffenhofer,
1984; Price and Paffenhofer, 1985; Berggreen et ai, 1988), and therefore, would
even have had less phytoplankton available in this environment dominated by
cells <10 um diameter (Sieracki et ai, 1993). The results of Dam et ai (1993) are
probably more a reflection of this food size limitation rather than of the mesozooplankton's biomass being slightly below that of the small copepods, and that
of the protozooplankton.
(iii) Protozooplankton, including microflagellates, dinoflagellates and ciliates
(Verity etai, 1993) favorably ingest particles in the range from 1/3 to 1/30 of their
body's equivalent spherical diameter (ESD, Hansen et ai, 1994) which implies
that the vast majority of phytoplankton cells during May 1989 being <5 um
diameter would be readily available to these protozoa. Among them, the ciliates
have been found to satiate at low food levels which means ingestion and growth
rates near their maximum may be obtained at regularly occurring environmental
food levels. For example, the ciliate Euplotes woodruffi reached maximum
ingestion rates near 20 ug C I"1 of the ciliate Metanophrys (Figure 1, recalculated
from Dolan and Coats, 1991). In situ oligotrich ciliates of 30 um ESD had
127
G.-A.Paffenhofer
exponential growth rates (u = 1.5-2 day 1 ) when chlorophyll concentrations of
particles of <11 um ESD were below 1 ug I"1 and nanoflagellates (usually the
ciliates' main food) were near or below 15 ug C I"1 (Nielsen and Ki0rboe, 1994).
Assuming that 1 ug of chlorophyll is equal to 40 ug C (Verity et ai, 1993) here
oligotrichs would attain these high growth rates at food concentrations near 55 ug
C H. These observations are supported by thefindingsof Vinogradov et al. (1976)
who observed for ciliates (infusoria) at their eastern most station in the equatorial
Pacific at 0.5-1.2 ug chlorophyll I"1 (Koblentz-Mishke and Semenova, 1977) an
ingestion rate of 427% of their body weight per day, and a weight-specific
production of 152% day 1 . Recent laboratory studies of the oligotrich genera
Strombidium and Strombilidium, however, resulted in lower growth rates and
higher food levels at which near maximum growth was achieved (Montagnes,
1996, Figure 4 therein). Strombidium siculum attained maximum exponential
growth rates of near u = 0.5 day 1 at -100 ug C I"1 of food, and S.capitatum was
near u = 0.75 day 1 at -1000 ug C I"1. One ought to consider, however, that
mixotrophy may have contributed to the observed high oligotrich growth rates in
the study of Nielsen and Ki0rboe (1994).
Finally, one ought to consider that oligotrich ciliates operating in oligotrophic
waters may have different perceptive capabilities of food particles and different
physiological rates as compared to those in neritic, mesotrophic or eutrophic
regions.
Under which conditions may metazooplankton reduce or control ciliates?
There has been repeated evidence that copepod nauplii have been ingested by
omnivorous copepods (copepodid stages and adults) in modest amounts at
environmental nauplius levels (Landry, 1978a; Paffenhofer and Knowles, 1980)
but copepodid stages have been preyed upon in far lower quantities (Landry,
1978b). There has been ample evidence that early juvenile and adult copepods
ingest heterotrophic protists (Stoecker and Capuzzo, 1990). As the metazooplankton ingested only rather small amounts of phytoplankton in the JGOFS
North Atlantic study, which was largely due to the overall small size of the phytoplankton, the questions arise to what extent they (i) can feed on the protozooplankton, and (ii) may be able to exert some kind of control over those they can
perceive and ingest (Sherr etal., 1986). Recent observations indicate that calanoid
copepods remove more ciliates than phytoplankton, although the former were
smaller and at a lower concentration than diatoms, i.e. preference for ciliates
(Verity and Paffenhofer, 1996). Exerting control means that the metazooplankton have a higher grazing rate (biomass X clearance rate/unit biomass) than the
protozooplankton's growth rate. In our case, if the mesozooplankton and metazooplankton <200 um mesh were considered both to graze at the same rate per
mg C of copepods (ignoring for now food size), they together would clear
between 577 and 719 1 irr 3 day 1 , resulting in exponential grazing factors g = 0.58
and 0.72. Therefore, control of proto- by metazooplankton during late May 1989
probably did not occur. These rates are below the average growth rates of k 0.78 of ciliates shown in Table 4 of Verity etal. (1993). Three other variables ought
128
Heterotrophic protozoa and metazoa
to be considered: (i) the clearance rate (ml h~l) increases with decreasing food
concentration for calanoids (Paffenhofer and Lewis, 1990); (ii) feeding on ciliates
by the estuarine copepod Acartia tonsa was far higher than on phytoplankton
(Saiz and Ki0rboe, 1995) indicating that a copepod with pronounced mechanoperceptive abilities could heavily impact the moving ciliates; (iii) this could be
partly offset by the presence of a wide variety of potential food particles which
reduces the ingestion rate (Figure 1). In our case, with small phytoplankton being
dominant, one could assume that the clearance rates supplied for these copepods
(from feeding on phytoplankton) could increase by -30-100% when feeding on
ciliates (Verity and Paffenhofer, 1996). In that case, the metazooplankton assemblage (almost exclusively copepods ranging from -38 to -45.5 mg C m~3) would
be able to regulate/reduce the ciliate assemblage. This, however, ought to be
interpreted with caution because the copepod species composition during late
May 1989 is not known. Data from Smetacek (1981) from Kiel Bight indicate that
when metazooplankton biomass was in excess of 25-50 mg C m~3 it coincided with
a decrease of the ciliates and heterotrophic dinoflagellates. Smetacek (1981)
stated 'when phytoplankton stocks are high, i.e. sufficient food available to
support a large metazooplankton stock, the latter apparently regulate the size of
the protozooplankton population'. This would imply that in the presence of high
concentrations of phytoplankton, copepods would appear to ingest protozooplankton preferably (Verity and Paffenhofer, 1996). Nielsen and Ki0rboe (1994)
calculated a potential clearance rate of a copepod assemblage on ciliates, and
found that larger ciliates (>50 um) throughout much of the year were regulated
by the copepods whose biomass ranged -12-35 mg C m~3. However, these authors
applied an unusually high clearance rate of 15 ml ug"1 of copepod dry weight
day 1 . The total copepod concentrations found reported for the North Atlantic in
May 1989 (38-45.5 mg C nr 3 ) are unusually high and are close to Smetacek's
(1981) data for metazooplankton in Kiel Bight. Such high copepod concentrations that allow regulation of phyto- and protozooplankton should occur rarely
in open ocean waters, unless high patchiness occurs. Such abundance also rarely
occurs in neritic waters except during periods following high phytoplankton levels
(Smith and Lane, 1988). However, tunicates are able to regulate phyto- and
protozooplankton and even calanoid copepod abundance because they can grow
faster than phytoplankton and protozoa and ingest calanoid eggs (Heron and
Benham, 1984; Paffenhofer et ai, 1995).
This leads to the final two questions: (i) why are protozoa, here ciliates, eating
more and growing faster than copepods; and (ii) why are ciliates in offshore
waters usually limited in abundance i.e. do not develop blooms, as compared to
copepods which at least seasonally or at upwelling events develop high abundances? A comparison of several variables may contribute to explaining the differences in feeding and growth rates.
(i) The range of particle sizes which is perceived and can be ingested is
narrower for nauplii (~4-ll um width) and early copepodid stages (-4-16 um
width) of small copepod species than for oligotrich ciliates of 30-40 um ESD
which regularly ingest particles from close to 1 um diameter to near half of their
ESD (Stoecker and Evans, 1985; Hansen et al, 1994).
129
G.-A.Paffenhofer
Early juveniles of small copepods such as Paracalanus sp. satiate at food concentrations and obtain maximum growth rates well above 100 ug C I"1 when
offered food compositions close to those found in situ (Figure 1, Paffenhofer,
1984). The larger the copepod, the higher the food level at which it will satiate
(e.g. Harris and Paffenhofer, 1976; Ambler, 1986). Oligotrich ciliates in field
studies obtained rather high growth rates near 55 ug C I"1 of food (Nielsen and
Ki0rboe, 1994). A significant percentage of these oligotrichs, however, were
mixotrophs. Oligotrich ciliates in the north Atlantic JGOFS study ingested on
average 240% of their body weight daily (Table I) and had an average exponential growth rate of k = 0.78 at 13.5°C at phytoplankton concentrations near
120 ug C I"1 (Verity et al, 1993). At similar food concentrations and temperatures,
calanoids cannot attain such growth rates. Feeding on a diverse phytoplankton
diet at 20°C near 126 ug C I"1 copepod stages I-V ingested daily on average 179%
of their body carbon content and had an average exponential growth rate of k =
0.49 (Paffenhofer, 1984; unpublished data).
Not only the quantity, but also the quality of food is significant. Whereas copepods, especially calanoids, regularly ingest diatoms which have a low nitrogen to
cell volume ratio, ciliates usually ingest particles (nanoflagellates) which have a
much higher nitrogen to cell volume ratio, i.e. the amount of food per unit volume
of particle ingested by a ciliate is higher than that of a copepod. Ciliates may also
ingest a higher percentage of heterotrophs than copepods. The nutritive value of
heterotrophs probably differs from that of autotrophs.
Protists select and ingest individual particles i.e. they can opt, in case of choice,
for the particle of highest quality. Copepods also select food particles, but as they
gather a perceived particle, accompanying lower quality particles can be collected
and ingested simultaneously (Paffenhofer and Van Sant, 1985). Also, a variety of
food particles in suspension will reduce the ingestion rate of calanoids (Figure 1,
Hansen et al, 1991) but not of protists. As shown above, calanoid copepods do
not appear to be able to obtain as much food per unit body weight per day as ciliates at similar food concentrations.
(ii) Since protozooplankton abundance does not increase infinitely, some type
of control mechanism must occur. Larger protists (ciliates) readily ingest similarly fast-growing smaller protists (Verity et al., 1993). Ciliates were thought to
have reduced abundance of microflagellates prior to 29 May 1989 (Verity et al,
1993), and in the middle equatorial Pacific were considered to be responsible, in
conjunction with low bacterial abundances, for a decrease in the flagellate community of Station 1461 (Vinogradov et al, 1976; Cruise 17 of R/V 'Akademik
Kurchatov' in 1974). Since the known predators of ciliates, i.e. copepods,
occurred in insufficient abundances during late May 1989 and also at Station 1461
to control ciliates, it is suggested that ciliates control each other by eating each
other, in a wider sense one would call it cannibalism (Vinogradov era/., 1977). It
was already stated earlier that mesozooplankton would most likely not be the
major predators of micrograzers in the subarctic Pacific i.e. of heterotrophic
protists (Frost, 1993), and that it could be probable that the larger microzooplankton would be likely predators. There is sufficient information in the literature that certain ciliates ingest other ciliates of similar or smaller size (Stoecker
130
Heterotrophic protozoa and metazoa
and Evans, 1985; Hewett, 1988; Dolan and Coats, 1991). Microflagellates are able
to ingest diatoms larger than themselves (Suttle et al, 1986). Oligotroch ciliates
in Kiel Bight ingested prey similar to their size (Smetacek, 1981). This information leads to the assumption that not so much metazoa but rather protozoa in
various regions of the ocean control protozoa at most times. This appears to have
occurred at Station 1461 although Vinogradov et al. (1976) only considered
feeding of the larger on the clearly smaller forms. As protozoa are able to ingest
each other, grazing pressure on bacteria (by nanoflagellates) and nanophytoplankton (by nanoflagellates and ciliates) should be reduced allowing them to
increase their concentration slightly, and thus serve again as food (i.e. true control
mechanisms!).
Whereas predation and cannibalism among copepods are partly limited by size
relationships (Landry 1978a,b) size appears to be of less significance concerning
predation among protozoa. This mode of community control, especially when
suitable prey is limited, should be considered as a means of increasing the persistence of protozoan communities. Protozoa including ciliates are known for
their limited starvation capabilities (D.K.Stoecker and P.RJonsson, personal
communication). However, a large percentage of ciliates, sometimes exceeding
50%, can be mixotroph, i.e. being auto- and heterotrophic (Stoecker et al, 1993).
A simultaneously or alternatively occurring means to provide survival of protozoa could be a reduction in metabolic activity which is thought to co-occur with
a drastic reduction of growth (Caron et al, 1990).
Other groups like heterotrophic dinoflagellates have not been included in this
evaluation but ought to be considered as predators on protists as well as on
metazoa as more information on their performance is being obtained.
Conclusion
An understanding of processes governing the existence and persistence of a
planktonic community requires an understanding of the operational activities and
potential performance ranges of its components. Summing components into
macrogroups like the meso- or microzooplankton will not lead to a true understanding of community functioning. The analysis presented here indicates that
observations on the basis of (i) genera, and (ii) groups of juvenile stages (e.g. late
nauplii, early copepodids) are the least resolution necessary to develop realistic
community models.
Acknowledgements
The author would like to express his gratitude to Evelyn and Barry Sherr, and
Peter Verity for reviewing this manuscript and providing constructive suggestions, to Vicki Patrick for typing the manuscript, and Suzanne Mclntosh for
drawing the figure. This research was supported by grants from the Department
of Energy (DE-FG02-92ER61419) and the National Science Foundation (OCE
94 15791).
131
G.-A.Paffenhofer
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Received on April 10, 1997; accepted on August 12, 1997
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