Download REVIEW Predation on Protozoa: its importance to

Journal of Plankton Research Vol.12 no.5 pp.891-908, 1990
REVIEW
Predation on Protozoa: its importance to zooplankton
Diane K.Stoecker and Judith McDowell Capuzzo
Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA
02543, USA
Abstract. Protozoa are an important component of both the nano- and microplankton in marine and
freshwater environments and are preyed upon by zooplankton, including suspension-feeding
cope pods, some gelatinous zoopiankters and some first-feeding fish larvae. The clearance rates of
suspension-feeding zooplankton for ciliates, in particular, are higher than for most phytoplankton.
For at least some suspension-feeding zooplankton, protozoans are calculated to be quantitatively an
important component of the diet during certain seasons. In laboratory studies, protozoan
components in the diet appear to enhance growth and survival of certain life-history stages or
enhance fecundity. These data suggest that protozoans are qualitatively as well as quantitatively
important in the diets of marine zooplankton. Most studies of predation on Protozoa have focused
on the euphotic zone in nearshore waters. Predation on Protozoa is expected, however, to be
particularly important both quantitatively and qualitatively in marine environments and seasons in
which primary production is dominated by cells <5 |im in size, such as nearshore environments after
the spring phytoplankton bloom, in oligotrophic waters, and in environments dominated by detritusdominated food webs, such as the deep sea. In detritus-dominated food webs, Protozoa may be a
source of essential nutrients and may thus facilitate utilization of bacterial and detrital carbon by
metazoan plankton.
Introduction
Protozoa are numerically an important component of the nanoplankton
(2-20 n,m size range) and microplankton (20-200 jim) assemblages in both
marine and freshwater environments [reviewed in Porter et al. (1985) and
Carlough and Meyer (1989)]. Although their potential significance in the diets of
both zooplankton and some fish larvae has been recognized (Pomeroy, 1974;
Sorokin, 1977, 1978, 1981; Porter et al., 1979; Kopylov et al., 1981; Conover,
1982; Poulet, 1983; Sherr et al., 1986; Fenchel, 1988; Sherr and Sherr, 1988),
until recently there have been little quantitative data available on predation of
Protozoa.
The planktonic Protozoa are a diverse assemblage and include the heterotrophic nanofJagellates, heterotrophic dinoflagellates, heterotrophic and mixotrophic ciliates, naked amoebae, and in oceanic waters, planktonic foraminifera,
acantheria and radiolaria. Loricae of tintinnid ciliates, skeletal material of
radiolarians and shells1 of planktonic foraminiferans are reported in the gut
contents of most taxa of planktonic invertebrates and fish larvae (reviewed in
Conover, 1982). However, the majority of planktonic Protozoa have no hard
parts and thus produce no recognizable remains. The role of Protozoa in the
diets of zooplankton and fish larvae has been largely ignored as most Protozoa
are not easily detectable in gut contents (Mullin, 1966; Stoecker and Govoni,
1984).
© Oxford University Press
891
D.K.Stoecker and J.M.Capuzzo
Observations from marine and freshwater habitats suggest that zooplankton
density has an important influence on the dynamics of protozoan populations.
Temporal studies of crustacean zooplankton and protozoan abundance in
temperate lakes (Porter etal., 1979) and coastal waters (Smetacek, 1981; Peinert
et al., 1982) suggest that zooplankton prey on ciliates and heterotrophic
dinoflagellates. This is supported by enclosure or mesocosm experiments in
which zooplankton density was manipulated. Elevated crustacean zooplankton
populations have been associated with decreases in heterotrophic nanoflagellates in estuarine experiments (Roman et al., 1988) and with a decrease of ciliate
populations in freshwater (Porter et al., 1979) and marine experiments (Sheldon
etal., 1986). At least at times, animal carbon is a large proportion of the natural
diet of suspension-feeding crustacean zooplankters usually considered to be
herbivorous (Kleppel et al., 1988). Most copepods appear to be omnivorous
rather than strictly herbivorous or carnivorous (Mullin, 1966; Corner et al.,
1974; Paffenhofer and Knowles, 1980). However, little attention has been paid
to the potential nutritional role of protozoans in planktonic food webs.
In the following sections, we will evaluate the potential importance of
Protozoa as a food source for zooplankton and fish larvae, review existing
experimental studies of predation by marine and freshwater planktonic
invertebrates and fish larvae on Protozoa, discuss the possible qualitative
importance of Protozoa in the diet of certain planktonic metazoans, and, when
possible, suggest potentially fruitful areas for future research.
Potential importance of Protozoa as a food source: considerations based on size
and abundance
Protozoa must be considered potentially important prey for zooplankton and
fish larvae as Protozoa are a major component of the particle-size ranges
efficiently utilized by these groups. Zooplankton differ in the particle size range
they can utilize. Most metazoan zooplankton do not efficiently utilize small
nanoplankton (2-5 ^m size range). Exceptions are rotifers and cladocerans in
freshwater environments [reviewed in Scavia and Fahnenstiel (1988) and
Stockner and Porter (1988)] and in eutrophic marine environments (Egloff 1988;
Turner et al., 1988), and mucus-net feeders including pteropods (Gilmer, 1974;
Silver and Bruland, 1981) and pelagic tunicates (salps, doliolids, pyrosomes and
larvaceans) (reviewed in Alldredge and Madin, 1982) in mesotrophic and
oligotrophic marine waters. Heterotrophic flagellates are probably an important
food source for zooplankton that consume small nanoplankton as they account
for 20-80% of the nanoplankton by cell number (Table I) and are particularly
important in the 2-5 \tsrn. size range (Geider, 1988).
Nanoplankton in the >5-20 jtm size range are efficiently utilized by most
suspension-feeding copepods (reviewed in Berggreen et al., 1988) as well as by
many rotifers and cladocerans and most mucus-net feeders. Heterotrophic
flagellates (probably mostly small heterotrophic dinoflagellates) and aloricate
ciliates undoubtedly contribute to numbers and biomass in the >5-20 u-m size
range in both nearshore and oceanic marine environments (Sherr et al., 1986;
892
Predation on Protozoa: its importance to zooplankton
Table I. Estimates of the percentage contribution of protozoans to the nanoplankton (2-20 \x.m size
range, unless otherwise noted) assemblage in surface waters
Environment
Contribution
Comments
Ref."
Marine
Mediterranean Sea
20-50% of cell number
3-10 |un size range flagellates and
ciliates
(1)
(2)
(3)
Sargasso Sea
43% of cell number
48-76% of cell number
Flagellates only
Flagelates only
North Sea
20-80% (av. 45%) of
cell number
Flagellates only
49% of cell number
52% of cell number
Flagellates only
Flagellates only
(2)
(5)
Coastal waters
25-55% of cell number
Flagellates only
(3)
Estuarine
60% of cell number
37% of cell number
Flagellates only
Flagellates only
(2)
(5)
Freshwater
Temperate pond
53% of cell number
Flagellates only
(6)
N. Atlantic
Continental shelf
(4)
"(1) Rassoulzadegan and Sheldon (1986); (2) Davis and Sieburth (1982); (3) Caron (1983); (4)
Geider (1988); (5) Davis et al. (1985); (6) Finlay et al. (1988).
Rassoulzadegan and Sheldon, 1986) but quantitative estimates of their contribution relative to phytoplankton to this restricted size range are not available.
However, because they are usually relatively abundant, they should be
considered a potentially important food for most suspension-feeding zooplankton.
Microplankton (>20-200 p.m size range) are utilized by some mucus-net
feeders (Gilmer, 1974; Deibel and Turner, 1985), almost all suspension-feeding
copepods (reviewed in Berggreen et al., 1988), by some raptorial copepods
(Paffenhofer and Knowles, 1980) and by somefirst-feedingfishlarvae (Lasker et
al., 1970; Last, 1978a,b; Cetta and Capuzzo, 1982; Checkley, 1982; Govoni et
al., 1983; Jenkins, 1988; and references cited therein). Heterotrophic dinoflagellates, ciliates and, in the open ocean, small sarcodines, make an important
contribution to numbers and biomass within the microplankton size category
(Table II).
At present, it is difficult to assess the potential contribution of Protozoa to the
diet of zooplankton because accurate estimates of the total contribution of
protozoans to nanoplankton and microplankton biomass are generally not
available. Few studies of protozooplankton have included all important taxa.
For example, heterotrophic dinoflagellates, which are an important component
of the nano- and microplankton in marine waters (Lessard and Swift, 1985;
Jacobson, 1987) have not been included in many studies. Nanoplanktonic
ciliates have often been ignored (Sherr et al., 1986). In addition, numbers and
biomass of certain protozoan groups have been severely underestimated in most
893
D.K.Stoecker and J.M.Capuzzo
Table D. Estimates of the percentage contribution of protozoans to the microplankton (20-200 u.m
size range, unless otherwise noted) assemblage in surface waters
Environment
Contribution
Comments
Ref."
20-50% of cell number
>10 p.m size range,
dinoflagellates and ciliates
(1)
1-30% microplankton
biomass
All microzooplankton,
including metazoa
(2)
=s20% phytoplankton
biomass
Ciliates only
Marine
Mediterranean Sea
South California Bight
Temperate estuary
Weddell Sea, Antarctica
Weddell Sea, Antarctica
Spring, 1983
Autumn, 1986
ice-covered station
open water station
Bellinghausen Sea and
South Georgia, Antarctica
(3)
10-25% phytoplankton
biomass
(4)
7-12% phytoplankton
biomass
(5)
15-23% phytoplankton
biomass
9-14% phytoplankton
biomass
(5)
(5)
—16% phytoplankton
biomass
(6)
Freshwater
Temperate pond
3-61% total plankton
biomass
-2-200 urn
(7)
"Rassoulzadegan and Sheldon (1986); (2) Beers et al. (1980); (3) Berk et al. (1977); (4) Bodungen et
al. (1988); (5) Garrison and Buck (1989); (6) Brockel (1981); (7) Finlay et al. (1988).
field studies due to methodological problems (Sorokin, 1981; Dale and Burkill,
1982; Gifford, 1985; Choi and Stoecker, 1989; Putt and Stoecker, 1989). It
seems likely that Protozoa often make up 20-50% of the biomass available in
the 20-200 jx,m size range (Tables I and II), but more complete and detailed
studies on the distribution and abundance of planktonic protozoans are needed
before the availability of Protozoa as a food source can be assessed accurately.
Experimental studies of predation in Protozoa
Although it is known that some rotifers (Pourriot, 1977) and some mucus-net
feeders (Gilmer, 1974) capture Protozoa, few or no experimental data are
available on predation by these groups on Protozoa. Among the zooplankters
capable of feeding on small nanoplankton, predation by cladocerans on
Protozoa is best described. In laboratory experiments, Porter et al. (1979)
demonstrated that the freshwater cladoceran, Daphnia magna, feeds at only
slightly lower rates on the ciliates Paramecium caudatum and Cyclidium
glaucoma than on phytoplankton. More recently, feeding by the marine
cladoceran, Penila avirostris on heterotrophic nanoflagellates (2-5 |un in
diameter) has been compared to feeding by this species on slightly larger
894
Predation on Protozoa: its importance to zooplankton
Table ED. Qearance of autotrophic and heterotrophic nanoflagellates by Acartia tonsa in laboratory
experiments (recalculated from Caron, 1984)
Nanoflagellates
Approx. size ((im3)
Qearance
(ml copepod"1 h~')
Autotrophs:
Isochrysis galbana
Dunaliella tertiolecta
48
157
<0.04-0.37
<0.04-0.18
34
42
0.08-0.41
0.22-0.47
Heterotrophs:
Monas sp.
Cryptobia marts
diatoms (Turner et al., 1988). Penila had a calculated clearance rate for the
heterotrophic flagellates of 1.4-4.0 ml animal"1 h" 1 , which was approximately
twice the clearance rate for small (4-12 |xm) diatoms.
In recent years, there have been a number of experimental studies of
predation by copepods on Protozoa. In laboratory experiments, the estuarine
copepod, Acartia tonsa, had comparable clearance rates for heterotrophic and
autotrophic nanoflagellates (Table III). In these experiments, although the
flagellates used as prey were relatively large, the clearance rates for both types
of flagellates were low. Higher rates might be expected in nature on similar-sized
prey. Kopylov et al. (1981) found that copepods and other suspension-feeders
had higher clearance rates for heterotrophic flagellates associated with particles
than for free-swimming flagellates. In both nearshore (Heinle et al., 1977) and
oceanic environments (Silver and Alldredge, 1981; Caron et al., 1982; Silver et
al., 1984), small flagellates and ciliates associated with detritus may be an
important food source for zooplankton. Laboratory data also indicate that
calanoid copepods can utilize large heterotrophic dinoflagellates (Klein
Breteler, 1980), but feeding rates are not available.
Laboratory experiments have demonstrated that marine copepods from a
number of genera can prey on planktonic ciliates (Table IV). Comparable data
for freshwater copepods are not available. Ciliates ranging in size from ~10 to
>100 (im long are cleared, usually at relatively high rates. Tintinnids, oligotrichs
and scuticociliates are all preyed upon. In general, the clearance rates fall
between ~1 and 5 ml animal"1 h" 1 , although lower and higher rates are
reported (Table IV). In experiments in which the copepods are simultaneously
exposed to both ciliates and algae, clearance of the ciliate is significantly higher
(2-10x) than of the alga (Table V). In mesocosm experiments, Sheldon et al.
(1986) observed a preference by the copepod Euterpina acutifrons for an
oligotrichous ciliate over diatoms or dinoflagellates. The higher clearance rate
for ciliates in both laboratory and field experiments may be due primarily to the
larger size of the ciliates than of the algae (Tables III and IV) or perhaps to a
perceptual bias for the ciliates due to their motility or to chemical clues (Price et
al., 1983; Jonsson and Tiselius, 1990). Whatever the underlying mechanism,
these data suggest that ciliates may often form an important part of the diet of
copepods in nature.
895
D.K.Stoecker and J.M.Capuzzo
Table IV. Clearance of ciliates by marine planktonic copepods in laboratory experiments
Copepod
Ciliate
Approx.
dimensions
(>m)
Acartia tonsa
Tintinnopsis mbulosa (T)a
Favella panamensis (T)
Favella sp. (T)
Tintinnopsis sp. (T)
Strobilidium sp. (O)
Strombidium sp. (O)
Balanion sp. (P)
Urotricha sp. (P)
48 x 148
82 x 265
65 x 150
32 x 65
50-60
42 x 43
32 x 34
9 x 12
3.9-12.0 (l) b
4.5 (1)
2-8 (2); 2.2-10.4 (3)
1.2-2.8 (3)
1.9 (3)
2.5-3.1 (3)
4.2-4.4 (3)
2.7 (3)
Acartia hudsonica
Eutintinnus pectinus (T)
20 x 150
0.2-0.4 (4)
Acartia clausi
Helicosomella fusiformis (T)
Favella tarakaensis (T)
Strombidium sulcatus (O)
23 x 110
77 X 210
30
0.3-0.9 (5)
2.0 (5)
1.4-26.3 (6)
Centropages typicus
Strombidium sulcatum (O)
30
5.4-58.1 (6)
Eurytemora affinus
Uronema nigricans (S)
9-17
Clearance
(ml copepod"1 h" 1 )
-0.1 (7)
°T = tintinnid; O = oligotrich; P = prorodontida; S = scuticociliate.
b
(l) Robertson (1983); (2) Stoecker and Sanders (1985); (3) recalculated from Stoecker and Egloff
(1987); (4) Turner and Anderson (1983), natural assemblage used as prey; (5) recalculated from
Ayukai (1987); (6) Wiadnyana and Rassoulzadegan (1989); (7) Berk et al. (1977), natural
assemblage used as prey.
Table V. Comparison of clearance of ciliates and phytoplankton (from assemblages containing both)
by marine planktonic copepods in laboratory experiments
Copepod
Relative clearance
Acartia hudsonica
E.pectinus' 2.6 x Gonyaulax tamarensisb
Acartia tonsa
Favella sp. 4-5 x Heterocapsa triquetra
Balanion sp. >5 x Chaetoceras simplex
Balanion sp. >5 x Pyramimonas sp.
(2)
(3)
(3)
Acartia clausi
S.sulcatum 4.4-4.9 x Prorocentrum micans
S.sulcatum 1.3-10 x Thalassiosira weissflogii
(4)
(4)
Centropages typicus
S.sulcatum 4.1-5.7 x Prorocentrum micans
(4)
"Ciliate dimensions given in Table I.
b
Approx. dimensions (\x.m): G.tamarensis 30-40; H.triquerta 15 x 22; C.simplex 5-10 (without
setae); Pyramimonas sp. 4-5; P.micans 13 x 47; T.weissflogii 10 x 15 (without setae).
c
(l) Turner and Anderson (1983); (2) Stoecker and Sanders (1985); (3) Stoecker and Egloff (1987);
(4) Wiadnyana and Rassoulzadegan (1989) (data from 2 h incubation).
This hypothesis is supported by grazing experiments which have been done
with natural assemblages (Table VI). In a subtropical estuary, Gifford and Dagg
(1988) calculated that Acartia tonsa derives from 3 to 41% of its daily ration from
predation on Protozoa (ciliates and flagellates >10 n-m). If these data are
recalculated using recently published, higher conversion factors from cell
896
Predation on Protozoa: its importance to zooplankton
Table VI. Protozoa as calculated percentage of the daily ration of copepods
Acartia tonsa
(subtropical estuary)
Acartia spp.
(temperate coastal waters)
Centropages hamatus
(temperate coastal waters)
Neocalanus plumchrus CV
(subarctic N.Pacific)
August
September
January
41% >10 jj.m ciliates and zooflagellates (l) a
11% >10 \x.m ciliates and zooflagellates (1)°
3% >10 (im ciliates and zooflagellates (1)"
Spring and summer
<l-10% ciliates only
(2)
~ 1 % ciliates only
(2)
11-18% ciliates and dinoflagellates
>5 [un
(3)
est. 28-59% from ciliates,
dinoflagellates and other protozoan
taxa
(3)
Summer
June
June
3
"(1) Gifford and Dagg (1988); carbon to volume ratio = 0.08 pg C u.m used for Protozoa and a
carbon/chlorophyll ratio of 30 used to estimate phytoplankton biomass in calculating ingestion rates.
(2) Tiselius (1989); carbon to volume ratio = 0.071 pg C p.m~3 used for Protozoa. Total carbon
ingestion calculated from egg production measurements.
(3) Gifford and Dagg (1990); carbon to volume ratio = 0.19 pg C fun""3 for ciliates and 0.08 pg C
u.m~3 for heterotrophic dinoflagellates and sarcodines. Carbon/chlorophyll ratio of 30 used to
estimate phytoplankton biomass.
volume to carbon for ciliates (Putt and Stoecker, 1989), the rations are 3-52%
(DJ.Gifford, personal communication). In temperate coastal waters, Tiselius
(1989) reports that Acartia spp. and Centropages hamatus derive an estimated
<l-10% and ~ 1 % , respectively, of their diet from ciliated protozoans (Table
VI). In the subarctic North Pacific, it is estimated that Neocalanus plumchrus
derives 11-16% of its ration from predation on ciliates and heterotrophic
dinoflagellates (Table VI) and as much as 59% if other heterotrophic flagellates
>5 jjun are included in the estimations (Gifford and Dagg, 1990). The results of
these three studies are difficult to compare because different methods were used
to estimate daily rations, widely different conversion factors were used, and
different size and taxonomic categories of Protozoa were considered (Table VI).
At least seasonally, however, Protozoa appear to be quantitatively important in
the diet of marine copepods in most nearshore and oceanic environments. The
same may be true for freshwater copepods, but comparable data are not
available.
In the marine environment, coelenterates and ctenophores are important
planktonic carnivores. Although most of these gelatinous predators are thought
to prey primarily on crustacean zooplankton and fish, some of them have feeding
modes which appear well suited to the capture of small-sized prey (Southward,
1955, Larson, 1988). Among the planktonic coelenterates, Aurelia aurita
appears to be adapted for feeding on small particles (Southward, 1955). This
species clears large oligotrichous ciliates from planktonic assemblages at rates of
up to several liters animal"1 h" 1 (Table VII). Tintinnids and small ciliates are
cleared at much lower rates. Unfortunately, comparable data for clearance of
897
D.K.Stoecker and J.M.Capuzzo
Table VH. Approximate clearance rates of estuarine and coastal suspension-feeding gelatinous
zooplankters for ciliates
Zooplankton species
Ciliate category
Clearance
(ml animal"1 h"1)
Amelia aurita
Tintinnids
<30 H-ra oligotrichs
30-50 (xm oligotrichs
50 fim oligotrichs
<42
(l) a
Usually <42
«91
316-5000
Mnemiopsis leidyi
Tintinnids
<40 (Jim oligotrichs
>50 M-m oligotrichs
<75
<71-430
50-214
(2)
"(1) Recalculated from data in Table VIII in Stoecker et al. (1987a); (2) recalculated from data in
Table VII in Stoecker et al. (1987b).
crustacean zooplankton have not been available, and therefore it is not possible
to evaluate the relative significance of protozoa in the diet of this important
coastal jellyfish (Stoecker et al., 1987a).
Among the ctenophores, experimental data on predation on Protozoa are
only available for the coastal species, Mnemiopsis leidyi (Table VII). This
species can clear aloricate ciliates at rates similar to that for the clearance of
copepods (Stoecker et al., 1987b). Since, at times, protozoan biomass can be
roughly equivalent to copepod biomass (Smetacek, 1981; Garrison and Buck,
1989), it seems likely that Protozoa can be, at these times, an important food
source for lobate ctenophores. Ciliates may be particularly important as prey for
larval ctenophores (Stoecker et al., 1987b). No data are available on predation
by oceanic ctenophores on Protozoa, although it seems likely.that many of the
lobate species may be capable of capturing microzooplankton.
Certain first-feeding planktonic fish larvae consume microplankton-sized
Protozoa (Lasker, 1975; Stepien, 1976; Last, 1978a,b; Hunter, 1981; Govoni et
al., 1983) but there is little experimental data on predation by fish larvae on
Protozoa* Stoecker and Govoni (1984) found that first-feeding gulf menhaden
select tintinnids over copepod nauplii in laboratory experiments. Winter
flounder larvae will initiate feeding within 24 h of hatching when small ciliates
are provided as prey (S.M.Gallager, D.K.Stoecker and L.H.Davis, unpublished
data). In addition to menhaden and winter flounder, first-feeding larvae of
northern anchovy, and a number of flatfish, have small mouths and are thought
to initiate feeding on small (<100 u.m) size particles (Blaxter et al., 1983); thus,
it is possible that in some situations Protozoa are an important food for them.
Overall, quantitative data on predation by zooplankton and fish larvae on
Protozoa are scarce and limited in scope to a small number of taxa of both
potential predators and prey. However, Protozoa have been reported in the gut
contents of most planktonic metazoan taxa (Conover, 1982). Little is known
about the utilization of heterotrophic nanoflagellates (including small heterotrophic dinoflagellates) by metazoans. Large heterotrophic dinoflagellates are
cleared by Neocalanus at rates equivalent to those for ciliates (Gifford and
898
Predation on Protozoa: its importance to zooplankton
Dagg, 1990). The situation for ciliates is somewhat better than for the other
protozoan groups. Although planktonic sarcodines are reported in the gut
contents of many oceanic zooplankters, nothing is known about predation rates
on sarcodines. Most of the available experimental data are for upper water
column, freshwater or marine coastal species. However, predation on protozoans may be particularly important in deep sea environments dominated by
detritus-based food webs and in upper water column, oligotrophic food webs in
which the bulk of the primary production occurs in the <5 ujn size class
(Pomeroy, 1974; Sherr et al., 1986).
Herbivorous or omnivorous crustacean zooplankton generally select Protozoa
over algae in grazing experiments and some Protozoa appear to be more
susceptible to predation than others (Tables IV and V). Copepods generally
clear ciliates at about the same rates as they clear large algal cells (Robertson,
1983; Tiselius, 1989; Gifford and Dagg, 1990). Gelatinous zooplankton that prey
on Protozoa do not appear to utilize similar-sized algae (Stoecker et al.,
1987a,b). These selectivities should have important consequences for ecosystem
dynamics (Smetacek, 1981; Frost, 1987) as well as on the nutrition of the
predators. The basis for these apparent selectivities is not well understood but
may include perceptual bias due to size, motility or chemical clues (Price and
Paffenhofer, 1985; Paffenhofer and Van Sant, 1985; Cowles etal., 1988; Butler
et al., 1989) as -well as mechanical defenses and escape responses of the prey
(Capriulo et al., 1982; Williamson and Butler, 1986).
Protozoa and the growth and survival of planktonic metazoans
During certairTTimes of the year or in certain habitats, phytoplankton biomass
does not appear to be adequate to support the standing stock of zooplankton.
Sorokin (1978) suggested that at these times, Protozoa may be a major food
source for zooplankton. In detritus-rich estuaries, ciliates appear to be
nutritionally important, both qualitatively and quantitatively, in the diet of
copepods when phytoplankton biomass is low or dominated by algal cells <5 p,m
in size (Berk etal., 1977; Heinle etal., 1977; Gifford and Dagg, 1988). In oceanic
environments, ciliates and other large protozoans also appear to be, at least at
times, quantitatively important in the diets of copepods (Table VII; Sheldon et
al., 1986; Gifford and Dagg, 1990).
Laboratory data indicate that Protozoa may be qualitatively as well as
quantitatively important in the diet of copepods. Klein Breteler (1980) found
that a number of marine copepods grew better when their standard algal diet was
supplemented with heterotrophic flagellates. The estuarine copepods Eurytemora affinis and Scottolana canadensis grow poorly when fed detritus with small
amounts of microbiota, but grow well when the detritus is rich in ciliates and
other protozoans (Heinle et al., 1977). Inclusion of tintinnids in the diet of
female Acartia tonsa can increase egg production by ~25% compared with a
pure algal diet (Stoecker and Egloff, 1987). It is likely that inclusion of Protozoa
in the diet of other 'herbivorous' zooplankton may simulate growth, but data are
lacking.
899
D.K.Stoecker and J.M.Capuzzo
There is some evidence that Protozoa may be particularly important to certain
early life history stages. Inclusion of tintinnids in the diet of ctenophore larvae
can increase early survival (Stoecker et al., 1987b). In laboratory rearing
experiments, survival of winter flounder, Pseudopleuronectes americanus,
through the 'critical' yolk-sac absorption period of larval development can be
increased up to 4-fold by provision of ciliates as food (S.M.Gallager,
D.K.Stoecker and L.H.Davis, unpublished data). Because Protozoa are, in
general, slower moving than most copepod nauplii, they may be differentially
utilized by certain invertebrate and fish larvae because they are easy to catch and
handle (Stoecker and Govoni, 1984; Stoecker et al., 1987b). More data are
needed to determine if protozoan abundance can affect survival of early life
history stages in nature.
Protozoa as a source of specific nutrients
It is possible that Protozoa are qualitatively important in planktonic food webs
because of their biochemical composition. In general, the C:N ratio in
heterotrophic marine Protozoa is lower than the ratio usually found in
phytoplankton or mixotrophic protozoa (Table VIII). It is possible that
Protozoa may be a particularly rich source of protein and amino acids, compared
Table VIII. Comparison of the C:N ratios (by weight) of marine planktonic bacteria, phytoplankton
and protozoa
C:N
Reference
4.1-5.7:1
3.7:1
Bratbak (1985)
(mixed culture)
Lee and Fuhrman (1987)
6:1 (recommended average)
3:1 to >15:1 (range)
Parsons et al. (1984)
Parsons et al. (1984)
Heterotrophic flagellates:
Paraphysomonas imperforata
Monas sp.
4.6:1-7.6:1
4.6:1
Goldman et al. (1985)
Borsheim and Bratbak (1987)
Planktonic ciliates:
Tintinnids
4.61-4.71:1
Verity and Langdon (1984)
Favella sp. (a tintinnid)
4:1
Stoecker and Sanders (1985)
Laboea strobila
(a mixotrophic oligotrich)
6-13:1*
Putt and Stoecker (1989)
Strombidium capitatum
(a mixotrophic oligotrich)
3-8:1*
Putt and Stoecker (1989)
Strobilidium spiralis
(a heterotrophic oligotrich)
3-4:1
Putt and Stoecker (1989)
Bacterioplankton
Phytoplankton
"Lower C:N ratios characteristic growth at low irradiances; higher ratios characteristic of growth at
saturating irradiances.
900
Predation on Protozoa: its importance to zooplankton
with phytoplankton and detritus, but data are lacking on the biochemical
composition of most taxa of marine Protozoa.
Most metazoans, including planktonic invertebrates and fish larvae, require
specific essential polyunsaturated fatty acids, sterols and amino acids in their
diet. Crustaceans, for example, have a limited capacity for de novo synthesis of
sterols (Zandee, 1966a; Kanazawa etal., 1971) and polyunsaturated fatty acids
(PUFAs) (Zandee, 1966b; Kanazawa and Teshima, 1977). Deficiencies in these
essential nutrients may result in reduced growth, survival and fecundity;
impaired development; impaired membrane functioning; and malfunctioning of
membrane-bound enzyme systems [see reviews by Sargent (1976), Langdon and
Waldock (1981), Capuzzo (1982) and Phillips (1984)]. It is likely that Protozoa
are an important source of some of these essential nutrients, particularly the
essential fatty acids and sterols which are lacking in non-living organic matter
and most, but not all, bacteria (Phillips, 1984; DeLong and Yayanos, 1986;
Yazawa etal., 1988).
Eukaryotic phytoplankton contain PUFAs, but the amounts and proportions
of the different types vary depending on taxon and growth conditions
(Harrington etal., 1970; Moreno etal., 1979; Volkman etal., 1981; Morentsen et
al., 1988). Mayzaud et al. (1989) examined seasonal changes in the sterol and
fatty acid composition of marine particulate matter and found major changes
associated with the taxonomic composition of the plankton as well as with the
growth and decline of phytoplankton populations. The degree to which seasonal
changes in fatty acid and sterol content affect the bioenergetics and growth of
planktonic suspension-feeders has not been explored. The essential fatty acids
20:5 a) 3 (eicopentaenoic acid) and 22:6 to 3 (docosahexaenoic acid) are required
for optimum growth in many marine animals and predominate in the tissues of
marine invertebrates and fish (Sargent, 1976; Joseph, 1982; Pillsbury, 1985).
With the exception of some of the heterotrophic flagellates, nothing is known
about the fatty acid composition of marine Protozoa. The heterotrophic
dinoflagellates, like the photosynthetic members of this family, are rich in 22:6 w
3 that stimulates growth in most marine animals (Harrington and Holz, 1968;
DiKarev et al., 1982). The heterotrophic chrysomonads and cryptomonads
usually contain appreciable amounts of 18:3 u> 3 and 20:4 co 6 (Holz and Conner,
1987). Although no data are available on marine ciliates, non-marine species
have been shown to have high lipid contents and to contain appreciable amounts
of PUFAs (Aaronson and Baker, 1961; Kaneshiro et al., 1979; Holz and
Conner, 1987).
In addition to PUFAs, most marine invertebrates and fish require dietary
sterols (Kanazawa et al., 1971; Teshima 1971a,b). Heterotrophic flagellates
(Williams and Goodwin, 1966; Alam et al., 1984) and ciliates often contain
appreciable amounts of sterols, but some of these differ in structure from the
dominant sterols found in phytoplankton and metazoans (Holz and Conner,
1987). It is not known to what extent metazoans can use protozoans to meet
their sterol requirements.
In addition to the essential fatty acids and sterols, most animals also require 10
essential amino acids in their diet. Amino acid deficiencies have been difficult to
901
D.K.Stoecker and J.M.Capuzzo
demonstrate in aquatic invertebrates or fish (reviewed in Phillips, 1984). Fyhn
(1989) has suggested that free amino acids (FAA) are an important energy
source for developing eggs and larvae of marine fish. An adequate supply of
FAA in foods for first-feeding larvae may enhance survival through the critical
period of yolk-sac absorption (Fyhn, 1989). Marine ciliates (Kaneshiro et al.,
1969) as well as other marine invertebrates characteristically contain high
intracellular concentrations of FAA (reviewed in Fyhn, 1989).
It is conceivable that inclusion of protozoans in the diet of zooplankton may
enhance survival and growth as Protozoa may be a rich source of essential
nutrients. Protozoa may be a richer source of these nutrients than most
phytoplankton. Both non-living organic matter and most eubacteria do not
contain or are very low in PUFAs and sterols. Thus, it is possible that Protozoa
may be particularly important as a source of essential nutrients in detritus-based
food webs (Phillips, 1984). Data are needed on the biochemical composition of
marine Protozoa relative to phytoplankton and detritus and on the fatty acid,
sterol and other nutritional requirements of zooplankton and fish larvae in order
to understand the qualitative as well as quantitative significance of Protozoa in
the diets of zooplankton.
Summary and conclusions
The limited data currently available indicate that predation on Protozoa is
nutritionally important to many invertebrate zooplankton and perhaps to some
first-feeding fish larvae. Suspension-feeding plankton, traditionally thought of as
'herbivores', in fact utilize a microbial food web that includes autotrophic and
heterotrophic components (Sherr and Sherr, 1988). Certain carnivorous
zooplankton and some fish larvae also ingest ciliates and other relatively large
Protozoa. Based on abundance alone, Protozoa appear to be of major
importance in planktonic food webs. Data are currently available, however, for
only a limited number of predator-prey combinations compared with the large
numbers of metazoans known to ingest Protozoa and the diversity of protozoan
taxa found in the plankton. In particular, data on predation on Protozoa are
lacking for freshwater zooplankton, open ocean zooplankton, non-copepod taxa
and early life history stages in general.
The few studies that have been conducted on zooplankton and fish larvae
predation on Protozoa suggest that both the behavior of Protozoa and their
biochemical composition may make them particularly valuable food sources for
certain species or life history stages (Heinle et al., 1977; Stoecker and Govoni,
1984; Stoecker and Egloff, 1987; Stoecker et al, 1987b). The role of protozoan
'supplements' to the diet in enhancing survival and growth or fecundity of some
zooplankton is particularly intriguing and needs to be explored.
Most of our information is from nearshore, euphotic zone plankton
assemblages. We have little information on predation on Protozoa from the
environments in which it is likely to be most significant both quantitatively and
qualitatively. In the oligotrophic ocean, Protozoa are thought to be particularly
important as a link between primary production and metazoan food webs
902
Predation on Protozoa: its importance to zooplankton
because the bulk of the primary production is by <5 (tin phytoplankton
(Pomeroy, 1974; Sherr et al., 1986). Most of the volume of the world's ocean lies
below the euphotic zone where fresh phytoplankton are scarce or available only
episodically. In these regions, detritus-based food webs are thought to be
important. For example, the majority of the bathypelagic calanoid copepods are
thought to be detritivores (Harding, 1974; Gowing and Wishner, 1986). Detritus
and bacteria alone, however, should be poor foods for metazoans because they
are generally low in essential fatty acids. The rich protozoan communities which
are often associated with sinking particles and marine snow (Silver and
Alldredge, 1981; Caron et al., 1982; Silver et al., 1984) may be a source of
essential nutrients and thus critically important to metazoan detritus-based food
webs in the deep sea.
Protozoa may also be important in nearshore food webs where or when
allochtonous organic matter augments local phytoplankton production (Sorokin,
1981), such as in detritus-rich estuaries during much of the year (Berk et al.,
1977; Heinle et al., 1977). In polar environments, primary production is limited
to a short season (Bunt and Lee, 1970) and detritus-based food webs may be
important, particularly in sub-ice waters or during the winter (Seki and
Kennedy, 1969; Buck and Garrison, 1988; Brockel, 1981). Protozoa may
therefore be both quantitatively and qualitatively important as a source of
nutrition for metazoans in polar food webs. We need to extend our observations
of predation on Protozoa to freshwater, oligotrophic, deep-sea and ice-covered
environments.
Acknowledgements
We thank S.M.Gallager, D.J.Gifford and M.Putt for their comments and
suggestions which greatly improved the manuscript. We thank D.J.Gifford and
S.M.Gallager for provision of unpublished data. Writing and research for this
review was partially supported by NSF grant OCE86-00684. This paper is
contribution no. 7385 from the Woods Hole Oceanographic Institution.
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Received on November 6, 1989; accepted on April 30, 1990
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