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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. 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