,
ICES Statutory Meeting
C.M. 1993/L: 13
Biological Oceanography Committee
PLANKTONIC PROTOZOA IN COPEPOD DIET: EXAMPLES FROM THE NORTH
ATLANTIC AND THE NORTH PACIFIC
by
Dian J. Gifford
Graduate School of Oceanography
University of Rhode Island
Narragansett, Rhode Island 02882-1197
USA
Telephone: (401) 792-6690FAX: (401) 792-6240
E-mail: D.GIFFORD (Omnet); gifford@gsosun1.gso.urLedu (Internet)
ABSTRACT
Planktonic Protozoa are ubiquitous and abundant in the euphotic zones of marine waters.
They funetion as important trophic intermediaries in pelagic food webs by repackaging
small bacteriaJ and algal cells into food items whiCh are accessible to larger consumers.
Although it has lang been observed that calanoid copeods which feed in the euphotic
zone tend to be omnivoraus, they are often treated as if they are exclusively herbivorous
in both mathematical models and manipulative experiments.
The objective of this paper is to compare the diets of two copepod species which are
Ca/anus finmarehieus dominates
characteristic of two targe oceanic areas:
zooplankton biomass in the North Atlantic and Neoea/anus p/umehrus dominates
zooplankton biomass in the North Pacific.
Experiments were performed at sea to measure ingestion of phytoplankton and Protozoa
by copepods. Experiments with Ca/anus finmarchieus were done as part of the
Marine Light-Mixed Layers (ML-ML) program in the North Atlantic. Experiments with
Naoea/anus p/umehrus were done as part of the Subarctic Paeific Ecosystem
Research (SUPER) program in the North Pacific. The experimental design consisted cf
classical on-deck bottle incubations in which the disappearance of prey was monitored.
Experimental treatments consisted cf the natural microplankton assemblage with copeods
added; control treatments consisted cf the natural microplankton assemblage alone.
A significant portion cf the diet cf both copepod spec1es consisted of ptanktonic
ProtozOB. 80th Ca/anus finmarehieus and Naoea/anus p/umehrus cleared
Protozoa at rates significantly greater than the rates at which they cleared phytoplankton.
Protozoa comprised up to 80% cf N. plumchrus carbon ingestion during spring. In
contrast, although clearance rates were high, protozoa comprised 20% cf C.
finmarehieus carbon ingestion in spring and 5% in Iate summer. The difference in diet
is attributed to the different phytoplankton environments in the two oceans.
INTRODUCTION.
The objective of this paper is to compare diets of copepods which dominate the
mesozooplankton biomass of two high latitude oceans, the North Atlantic and the oceanic
subarctic Pacific. The copepods are Neocalanus plumchrus in the North Pacifie and
Ca/anus finmarchicus in the North Atlantic.
Protozoa in marine ecosystems. Nano- and miero- plankton are defined on the basis
of size as organisms 2-20 /-Im and 20-200 /-Im respectively (sensu SIEBURTH,
SMETACEK and LENZ, 1978). The nano- and miero- zooplankton constitute the animal
components of the nano- and miero- plankton. Herein, the two categories are termed
collectively "microzooplankton for simplicity. These operational categories contain a
diversity of taxa including ciliate, heterotrophie flagellate, heterotrophie dinoflagellate, and
sarcodine Protozoa and rnetazoan nauplii. Mierozooplankton are ubiquitous and
abundant in the euphotic zones of marine waters (BEERS, 1978; CONOVER, 1982), but
have not been studied extensively in oceanie waters untillast decade.
U
Planktonic Protozoa perform a number cf functions in marine ecosystems. They are
major grazers cf phytoplankton (e.g., GIFFORD, 1988 and studies cited therein) and
bacteria (e.g., SHERR, RASSOULZADEGAN and SHERR, 1989). They are major
recyclers cf nutrients (e.g., CARON, 1991). Sy virtue cf endosymbiotic relationships, a
number also function as primary producers (e.g., STOECKER, 1991). And, they function
as atrophie link between mierobialloop organisms and higher order consumers (e.g.,
STOECKER and CAPUZZO, 1990; GIFFORD, 1991). This last function is the focus of
this paper.
Protozoa in copepod diet. It is now recognized that planktonic Protozoa function as
important trophie intermediaries in pelagie foOO webs by repackaging small bacterial and
algal cells into foOO items which are accessible to !arger consumers. Although it has
long been observed that caJanoid copepods which feed in the euphatie zone tend to be
omnivorous (e.g., LEBOUR, 1922; DIGBY, 1954; ANAAKU and OMORI, 1963;
PAFFENHOFER and KNOWlES, 1980), they are often treated as if they are exclusively
herbivorous in both mathematical models and manipulative experiments. OuaJitatively,
direct observation of gut contents reveals that tintinnid ciliates, whose hard Ioriese are
preserved after digestion, are ingested by many caJanojd copepods (e.g.,LEBOUR, 1923;
MARSHALL and ORR, 1955; MULLIN, 1966; ZEITSCHEL, 1967; HARDING, 1974), and
tintinnid loricae have been observed in copepod fecal pellets (TURNER and ANDERSON,
1983). The usually more abundant aloricate ciliates da not possess hard parts which
survive digestion and are not easily observed in guts er fecal material.
Laboratory studies using cuJtured prey have documented consumption cf tintinnid
Protozoa by a number cf calanoid copepod species, and demonstrate the potential
importance cf these prey in the diets cf their consumers (reviewed by STOECKER and
CAPUZZO, 1990; GIFFORD, 1991). Recent studies emptoying natural preyassemblages
2
r-
~
',.>$ ..' ..... ,.,-:.. ' .
,
demonstrate that calanoidcopepods consume a number of protozoon taxa urider field,
as weil
laboratory, conditions ät rates and: in quantities which äre physiologically
important to the consumers. The evidenceiÖdate comes from several copep6d genera
and a diversity of marine environmentS., GIFFORD and DAGG (1988) foundthat Acartia
Cl n a fernales in, ä. subtröpical estLi~rY öbtäined" significant nUtrttion from protoZoon prey,
wtth Proto:z?s nlSking ~,greater coritribution to, diet during summer when large
phYtoplankton ceUs ware räre: BARTHEL (1988) observed that latestage c6pepodid and
famale Ca/anus finmarchicus,C. giacialis and C. hyperboreus in a diversity of
environ'mEmts in tl1ä, Greenlarid Ses consumed ciliates. and heterotrophie dinoflagellates
proportiomite tO thair Btiundal1ces in situ. Because of their large size, ciliate Protozoo
constitutäda significänt proportion of the, copepOds'carbon intake, even though they
were not as numerically abluidiint es smalJer phytoplankton cells.
a.s
t s
•
siZe.
Recent studies Cf freshwater Protozoa suggest that, in addition to being of suitabie
they are rich in dietäry, components required by suspension-feeding copepods. Most
metBZOanS require specific essential polyunsaturated fatty, acids (PUFAs), sterols arid
amino acids in their dietS (reviewed by PHILLIPS, 1984; STOECKER and CAPUZZO,
1990). The Iimtted data 6n the biochemical composition cf manne protozoa suggest
ttiat they are lich in nttrogen-centaining compounds;theirG:N ratios are lower.than the
ratios characteristic cf phYtoplankton '(reviewed by S,.OECKER arid CAPUZZO, 1990;
GIFFOAD, 1991). Althougli the fatty acid biochemistry cf marine ciliates has not bee"
studied, tWo freshwater ciliStes, Paramecium sp. and Tetrahymena sp., contain
significant concentrations ofHpids and PUFAs (NOZAWA and THOMPSON,1979; HOLZ
and CORNER, ,1987; AARONSONand BAKER, 1961;KANESHIRO,' BEISCHERL;
MEAKEL arid RHOADS, ,1979). ,Amino acids most likely to bedeficierit in mE)taZean prey
include methionine, histSdine, lysine arid arginine. Protozeans appear t6
the~e as
free amino acids (FAAs) (KIDDEA, 1967) and thus should provide a
source cf
FAAs for their consumers (FYHN, 1989).
have
bB.lanced
Consumptiori cf protozoan prey mayaffOOt copep6d condition and productlon. Acartia
tonsa females prOduced .... 25% more eggswhen tintinnid ProtozOa er rotifers were
includad in ttte ,diät (STOECKER ,and EGLOFF1987). UncJer corditions,öf pr.OIon~
cultiVätion the bOdY size cf Pseudoca/anus e/ongatusinöreased significantlywhen
heterotrophicflagelläte OXYrrhis mar/na was included in th8 diet, in contrast to
diet consisting s()1S1y of, phYtoplankton (BRETELER, SCHOGT and GONZALEZ.1990).
GATTEN, SARGENT, FORSBERG,O'HARA äl1d CORNER (1980) related 8gg produdion
by Ca/anus finmarchicus to the level Cf lipid in phytoplanJ<tori arid itS assimilation by
the copepods., '" tf Protözoa,in general" are Iipid-rich, they are likelY to corltJ'ibute
significantly to the metabolismof their consumers, pärtiCulSrlygenera such as Ca/anus
and Neoca/anus WhiCh aceumulate lipid rasaNes during much of their life cycle.
the
a
Ecologieal setting.
North
paciiic. exPerimentS
in the North Pacmc were performed as one
3
,
component cf the SUPER (SUbarctic Pacific Ecosystem Research) program, an
interdisciplinary effort supported by the U.S. National Science Foundation. The oceanic
subarctic Pacific OCean is characterized by relatively constant, low levels cf chlorophyll
a throughout the annual cycle, with concentrations rarely exceeding 0.5 #Jg L- 1 • Despite
a pulse of primary production in spring, phytoplankton does not accumulete as a bloom
(McALLISTER, PARSONS and STRICKLAND, 1960; CLEMONS end MILLER, 1984;
SAMBROnO end LORENZEN, 1986). The phytoplankton community is dominated by
small cells (BOOTH, LEWIN and NORRIS, 1982; TAYLOR and WATERS, 1982), with
cells < 5 #Jm contributing approximately 2/3 cf phytoplankton carbon (BOOTH, 1988;
BOOTH, LEWIN and LORENZEN, 1988). Although major nutrient levels are reduced
during summer, nitrate is never depleted and concentrations remain high throughout the
year (ANDERSON, LAM, BOOTH and GLASS, 1977; WHEELER and KOKKINAKIS,
1990). The distinguishing physical features cf the region are a low-salinity layer of
surface water located above a permanent halocline at - 130 m, which strongly inhibits
deep convective mixing.
The mesozooplankton community of the region is dominated by three endemie copepod
species cfthe genus Neoea/anus: N. p/umehrus (Marukawa), N. f1emingeri Miller
and N. eristatus (Kroyer). Their life cycfes in the ares are such that females produce
eggs using lipid resarves aequired during the previous growing sesson. The eggs are
released at depth during winter or early spring. The eggs develop to nauplius stage VI
or eopepodid stage I as they ascend to the surface where they feed and develop further
to copepodid stage V. Having accumulated lipid, copepodid stage Vs make an
ontogenetic migration to deep water and remain there until they mott to adutts, reproduce
and die in Jate fall or winter (MILLER, FROST, BATCHELDER, ClEMONS and CONWAY,
1984; MILLER and CLEMONS, 1988). These Iarge-bodied copepods are the Iargest
standing stock cf biomass in the system from Iate wrnerthrough spring (FULTON, 1978;
1983). During their growing season, copepodid stages cf N. p/umchrus is restricted
almest entirely to the water cotumn.above the seasonal thermocline (MILLER and SUPER
GROUP, 1984).
The classical explanation for the observed constant levels cf chlorophyll in the oceanic
subarctic Pacific posits that, because cf the dominant copepods' unique life history
pattern, phytoplankton growth and copepod grazing are in balance in the spring, with
copepods cropping the phytoplankton as soon as it is produced (McALLISTER,
PARSONS and STRICKLAND, 1960; HEINRICH, 1962; PAASONS and LEBRASSEUR,
1968; MILLER, FROST, BATCHELDER, CLEMONS and CONWAY, 1984). However,
studies condueted during the first SUPER expeditions to the area in 1984 demonstrated
that the copepod community, in toto, does not exert sufficient grazing pressure to
balance phytoplankton growth (MlllER and SUPER GROUP, 1988; LANDRY and
LEHNER-FOURNIER, 1988; DAGG, 1993) during spring and esrty summer when the
Iarge.bodied copepods are present in surface waters. Nor does this "major-grazer
hypothesis" explain the persistence cf balance after the copepods enter diapause and
leave the euphotic zone.
4
The fee.ding appendages Cf Neocalanus spp. are structured so that the copepods are
capa~le ,of capturing partides, > 2-3
butttiey clear cells < Sill!' with reduced
efficiency (FROST, LANDRY and HASSETT' 1983). Hence, ttleyare 8ble to utilize some
of the small cells which. dominatS the sUbaretic Pacific phytoplankton. However, in the
dilute environment of ttle oceanie subarctic Pacifie" Neocalanus spp. are unable to
consume,sUfficient phytoplank~6nto maet even basic respiratory requirements (M1LLER
and SUPER GROUP, 1988; LANDRY and LEHNER-FOURNIER, 1988; DAGG, 1991).
In contrast, ,in öther high latitude environments where ständing stocks of plant cells are
higher, end phytoplcmkton cell sizes are lärger, Neocalanus spp. consume
phytoplankton 8t rates eind in amourits sufficient to meet metabolic arid reproductive
needs (DAGG, VIDAL; WHITLEDGE, IVERSON and GOERING, 1982; DAGG and
~MAN, 1983).
.
pm,
•
North Atlantic. experimentS in the Nol'th Atlantic were performed as a component
of the Marine Light- Mixed Layer~ (ML-ML) program, a large multi-investigator prcigram
suppoited by the U.S. OffiCe cf Naval Research. The ML;.ML study site is 16cated in ttie
high latitude Norttl AtlantlC at 59°N, 21OW, south of the Subarctic Front, an area
chamcterized by eXtreme seasonal forcing of biology and physiCs. Convec:tive cooling
of the ,. water column. during winter produces ,a deep mixed Iayer Cf at least several
hLindred meters, which mixes new nutrients into the system (ROBINSON, et
1979):
Irtadial1cS.arid phytoplankton stariding. stocks, arelow, and phytoplankton growth ,is
believed to be very low. With
6nset of. stratificationin - April, stariding stOcks of
chlorophyll increase (WILLIAMS arid HOPKINS,197~), and a prominent bloom typicallY
ÖCCUfs in May, ,with '. chllorophyll.levels reaching 2-5 /.Ig L· 1• .CläSsiCalty, .the bloom has
been described as dominated by diatoms (e.g., COLEBROOK, 1982): However, the
bloom in 1991 was dominated by Phaeocyst/s pouchettii: Ca/Clnus spp.apPäar
in the euphotic zone at thistime, where theyare believed to produCe more than one
generation (CONOVER, 1988). It appears that their graZing has Iittle impact on the bloom
arid that most cf the phytoplankton sink to the bottem (P~RSONS and LALLI, 1988).
Transition to the summer phytopläriktoiicommul1ity, char8ct E3 rized by dirioflagellates and
Rhizoselenia spp.; occurS in June, when euphausiids, siphonöphores and ctenophores
also appear (e.g. COLEBROOK 1984; WILLIAMS and LlNDLEY, 1982). Maximum water
column stability occurs in August.
sI.
ttle
•
METHODS.
North PacifiC experiments. Methodsfor ttie Norttl.Pacific,experiments are de~nb~d
in detail
GIFFORD and DAGG (1991) snd G1FFORD (19938; 1993b). ExPerimentS
were done"at oCean Stations P (50 0 N, 145 'W) arid R (53°N, 14? OW)inttle subaretic
PacifiC Ocean during June, 1987. N~ plumchrus CV and were collected by vertical
hauls of a "bag sampleru (C.B. MilIer, unpublished). CopeP6dswere colteeted from
depth 6f 50, m through the mixed l8yer . (mixed .layer depth == 35~,40 m). Th9 ne~
equipped with eilarge volume, nori-filtSring cod end, (REEVE, 1981) which collected
copepOds in gö6d condition, with their plumose selSe intSet. C0Pepods were sorted
in
a
Was
5
directly from the aquarium cod ends into 2-liter polycarbonate incubation bottles with
plastic soup Iadles.
North Atlantic experiments. Experiments were done in May and August 1991, tollowing
methods described by GIFFORD (1993a) and GIFFORD, FESSENDEN and GARRAHAN
(submitted). The May experiments were done after the peak cf the spring bloom.
Copepods were collected at night by vertical hauls cf a 335 lJTT1 mesh, 1-m diameter
closing ring net. Ca/anus finmarchicus were sorted under a dissecting microscope
using a wide bore pipette and transterred to 1-Liter polycarbonate incubation bottles
containing seawater collected tram the middle cf the mixed Iayer.
All experiments. Seawater containing the microplankton assemblage was collected trom
the middle cf the mixed layer in Go-tlo bottles. Water was siphoned gently through wide
bore silicon tubing into a 20-liter polycarbonate carbuoy, mixed gently with a teflon
paddle, and siphoned through silicon tubing into polycarbonate bottIes. The Go-flo
bottles, incubation bottles and tubing were cteaned according to the protocol cf
FITZWATER, KNAUER and MARTIN (1982). Temperature and salinity were recorded
trom CTD traces obtained immediately betore the Go-tlo bottles were deployed.
The experimental design consisted cf an experimental treatment in which the
microplankton prey assemblage was incubated in bottles with copepods and a control
treatment in which bottles contained only the prey assemblage. Microplankton sampies
were collected trom each incubation bottJe at the beginning and end cf each experiment:
one liter of seawater was preserved in 20% (v Iv) acid Lugols solution (THRONDSEN,
1978) for later processing by inverted microscopy. Chlorophyll sampies were collected
tram all treatments at the beginning and end ot all Ca/anus finmarchicus experiments,
tor later analysis by tluorometry. After addition cf the copepods to experimental
treatments, all bottles were topped up with microplankton assemblage, sealed with
Paratilm to exclude airspace, which destroys delicate aloricate ciliate prey, and capped.
The bottles ware rotated slowly along their vertical axes in an on-deck incubator whose
temperature was maintained by tlowing seawater. Ambient light was dimmed by covering
the incubator with a translucent tarpaulin. Experimental duration was 24h. Copepods
were acclimated to the experimental conditions tor 1-2 hours betere initial treatments were
harvested. Copepods were collected throughout all cruises tor ancillary rneasurements
of dry weight. Initial experimental conditions are summarized in Table 1.
The details cf microplankton sampie processing are discussed by GIFFORD and DAGG
(1991), GIFFORD (19938), and GIFFORD, FESSENDEN and GARRAHAN (1993b), and
are not repeated here except to note that the experimental design requires that absolute
numericaJ abundances cf the protozoan prey be measured and that the volumes cf the
prey items be estimated in order to calculate their carbon content. Success depends on
separating the Copepod teeding signal trom counting variation. Because the coefficient
cf variation cf the counting method is - 20%, optimalty the copepods should clear - 40%
cf the volume in the incubation bottles (GIFFORD. 19938). Statistically significant
6
•
•
"
... .
chäi1ges in atiundänce are, resolVed in preycategories cOl1taining abundant c81ls~ Le., in
which 100-200 6el15 are counted (VENRICK ,1978). Per capitacl,earance rates of
copepods on microzooplankton: in the most abundant size categories ware calculated
trom FROST's (1972) equaticins. Because only a tew of the 50 t070 prey categories
pressl1t in aach experiment, contSined sufficient numbers of individuals to permit
calculaticin of C1eararice rates only categories containirig> 100gells were used to
calculate clearance 'rates. A, grand, mean Of clearance rates on these abundant prey
categodes wasthen cal6ulateä Total ingestion was ealculated by multiplying clearal1ce
rate by the ,initial Standing, Stock of ProtOIoa (MARIN, HUNTLEY and FROST ,1986).
Descriptive steltistics of feeding rates were calculated according to SOKAL and ROHLF
(1981).
RESULTS.
NOrth
pscific.
Microplankton assemblage. The Stcinding stOck of chlorophyll Si averaged 0.4
pg L· during June, 1987. The phytoplankton assemblage was, d6minate(j by, cells <5
pm (BOOTH, LEWIN arid POSTEL;,1993). Ttiä protozoan assemblage collected from the
middlEi of the miXed layerat statiOns P arid R,was dominated numerically byaloricate
ciliates, primarily oligotrichaus forms. The predatoryaloricate cilate Didlnium Sp.
present in, low abundances. , Tintinnidciliates comprised, er1, average, ,2.25%of total
ciliates, with greater atiundances st station R later in June. "ether heterotrophie
includedthecate dinoflagelJates > 20 IJm, primariIYProt6perldlnlumspp., and athecate
dinoflagell8tes > 20 pm, ,primarily, Gyrodlnium spp. ,Hadiol8nans, made a small
cöntribution to microzooplcmkton numbers. Protozoan ciütion biomass rangedfrom 1.25
to 5.27 IJ9C i..- 1 (mean = 3.32 j.tgCL·1 ± 1.28 s.d.). Radiolarians made
small
contritiuti6n (mean = 1.29%) tö protozoan biomasse
1
was
taxa
a
•
, Copepod feeding rates. Tnerewas no copepOdmortality in any cf ,the
experimentS. Neocalänus plumchrus cleared Protozoa at rates rangingfrom 7.18 to
39.04 ml copepoCf 1 h-1 (mean = 22.73 ± 11.33 s.d.). Phytoplankton cellS > 20 pm were
cleared at the same rates si; protozoon prey. 55% of theincubation volume was C1eäred
on average in the ex rime ritS.
mean groWth coeffieient (k in FROST's (1972)
equations) of the protozoan assemblage was, not significiintly different from zero (friean
=,.:,0.003 h-1 ±.O 1 s.d) foi' all experiments. The mean grciZing coefficient (9 in FROST's
(1972) equatioris)was 0.02 h·'±0.01 s.d. Neocalanus plumchrus ingeSted 0.67
to 3.91,IJg protoZoai1-C c0PePOd- 1 d-1 (mean = 1.58 iJgC ± 1.12 s.d.) (Table 2),
accounting for -77% Cf itS nutritiOn (Figure 1).
Pe
The
NOrth Atlantic.
#19 L-\
assembläge.in
May, the 'standingstOck of chlorophYll a
with 67-84% < 20;"m following the declirie of the Phaeocystls
, MicröpJ8nkton
averaged 0.90
7
bloom. During August, the standing stock of chlorophyll a averaged 1.39 Ilg L', with 6783% < 20llm. Nitzschia spp. dominated the phytoplankton> 20 11m numerieaJly in May,
with centrie diatoms and thecate dinoflagellates present at lower levels. In August, the
microphytoplankton assemblage was more diverse, consisting cf Rhizose/enia spp.,
and a number of thecate and athecate dinoflagellates. The mierozooplankton was
dominated by aloricate ciliates, primarily oligotrichous torms, during both May and August.
Tintinnid ciliates comprised < 1% of total ciliafes in both months. Heterotrophie
dinoflagellates were present during bOth seasons, with the heterotrophie genus
Protoperidinium abundant during May. Numerical abundances of Protozoa were
approximately twiee as high in August as in May.
Copepod feeding rates. There was no copepod mortality in the experiments.
Ca/anus finmarchicus cleared Protozoa at mean rates ot 7.76 ml copepocf' h-' ±
0.01 s.d. in May and 6.17 ml copepoef' h-' ± 1.20 s.d in August. Phytoplankton cells
> 20 11m were cleared similar rates to protozoan prey. Chlorophyll was cleared at mean
rates ot 2.12 ml copepod" h-' ± 0.00 s.d. in Mayand 1.77 ml copepod-' h" ± 0.41 s.d.
in August. The mean growth coeffieient, k, cf the protozoan assemblages was 0.01 er'
in May and - 0 cf' in August. The mean grazing coeffieient, g, was 0.05 cf' in May and
0.08 cf' in August. Total ingestion was 1.081lg C copepod"' cf' in May. Cf this, 89% was
derived trom phytoplankton and 11% trom Protozoa. Total ingestion was 2.7 Ilg C
copepod- 1 d- 1 in August, with 96% derived trom phytoplankton and 5% derived from
Protozoa (Table 2; Figure 1).
DISCUSSION.
The experiments document consumption ot Protozoa by Neoca/anus p/umchrus CV
in the subarctic Pacific environment and by Ca/anus finmarchicus CIV and CV in the
high Iatitude North Atlantic. 80th copepod species cleared protozoan prey at rates
considerably higher than those at which they clear bulk chlorophyll a.
The protozoan assemblages in the North Pactfic and the North Atlantic were typical cf
those observed in ether oceanic areas, with oligotrich ciliates dominating the
mierozooplankton numericalty and in terms cf biomass (e.g., BEERS and STEWART,
1971; BEERS, REID and STEWART, 1975; HALLOAL, 1953; TANIGUCHI, 1984).
On the basis of body weight and Iipid content, Neocalanus plumchrus in the subaretic
Paeific in 1987 required 5.1 Ilg c d-' to satisfy basic respiratory requirements. The
calculated requirement tor N. p/umchrus is similar to DAGG's (1991) estimate of 6.2
IJg C d-'. In the experiments described above, N. plumchrus obtained at most 3.91JgC
d-' from the planktonic Protozoa enumerated in the experiments, accounting tor - 77%
of basic respiratory requirements. Adding the 1-21JgC cf' that the copepods obtain trom
bulk phytoplankton (DAGG and WALSER, 1987), N. plumchrus nearly satisfies its daily
respiratory needs. On the basis cf body weight, Ca/anus finmarchicus in the North
8
•
.)
~.,
.
",
1
Atlantlc in 1991 required on the order of 1.4 .I1g C d to, satisfy, basic respiratory
requiremeri1S (IKEDA, 1970).. In May," after, the decline, of the spring bloorri, C.
finmarchieus fell short of this amolmt, obtaining -80% cf its daily respiratory needs.
In August, C. finmarchicus obtäined -200% of daily respiratory needs.
Due to fecal and excretory lasses, respiratorY demands are considerably less than the
ainount of ingestion required for growtti. For N. plumchrus in the North Pacific arid
Ca/anus finmarchicus in the NorthAtlantic in May t6 grow and repr()duce, additional
ingestion must occur. ,This inay be obtained fram a number of sources. It is Iikely that
the carbon content of the Protozoa is higher than calculated for two reasons. First, the
rrlicroscopic measurements of protozoan dimensions are conservative: irregular structures
which are difficult t6 rrieasure, such as ciliate oral membranelIes and tBiis, are, not
included .in organismal georrietr;'. Secend, the carnon biomass calculated from PUTI
and STOECKER's (1989) empirical relationship is conservative. ,20% (v/v) acid Lugols
solution was chosen as a fixative because it preserves virtLially all planktonic ciliates and
athecate dinoflagellates, organisms for which preservation can be problematic (GIFFORD,
1985; 1992). However, the preserved cells shrink dramatically. bya large, but
inconsistent, factor, losing, as much as 50%of, their volume (GIFFORD, 1993a).
Prolozoän earbori biomass is not corrected in this fa6tor, and is Iikely to be considerably
higher thar! calculated. Additional nutritional sources must also be considerE3d.
Heterotr()phicflagellates < 20 pm, are an obvious additional nirtritionaJ, souree, not
examined directly in the experiments. These organisms were abundant in the mixed layer
ef the subarctic Pacific during June,1987 (BOOTH, lEWIN and POSTEl,1993). From
BOOTH, lEWIN and POSTEl'S .(1993) datä for tlle. abundance of h~terotrophic
f1ageltates at" a depth ,of 20" m in the water column, arid, assuming that heterotrophie
. fl8g81late5 are C1eared from the water at
same rate as eiliates and large phytopl8nkton
cells, it is clear that heterotrophie f1agellcites < 20pin contribute potentially as much as
ciliates and larger heterotrophie flagellatesto the diet .of N. p/umehrus. Although
heterotrophie flagell8tes ware not enumerated in.the North Atlantic experimens, a.similar .
argument rriay be made for their role as prey items for C. finmarchicus. ,Copepod
nauplii are anottler possible m.itritional resourcs. They were present at levels cl, 10to 80
1
L- , in .the ,microplankton assemblages of both ciceans. (Gifford, unpu~lished. data),
abundances too low to perrnit calculation of ingestion in the exPerimentS. Everi ,if
ingestion of these large partieles ocCurs asrare eventS" itwill contribute significantly to
consumer nutrition." Furttler, exPeriments perforrned in bettles da. not resolve eRisodie
eventSsueh as cOPepods feeding cin patches of preY. Sueh rare,large m~als may weil.
be an importarlt nutritional resoures in natUre. Consideririg these additiomil nuti-itionäl
resources, Neocalanus plumehrus and Ca/anus finmarchieus appeartci be ahle
to meat their metabolie andreproductive requirementS in their respective environmentS.
tIle
•
In the eontext of ecosystem furiCtion, it is cf interest to eonsider the RC?tennalimpa6t of
consurrier feeding activities on prey populätions~ N. p/umchrus eleäis Protozoa at a
meän rate Of 0.55 L coPePod· 1 d·1• The ObServet! number Cf uNo ,ij/umchhrusequivalentSU Le., total copepod äbundance expressed in the eurrency Cf N~ p/umchrus
9
CVs (MILLER and SUPER GROUP, 1988), in the mixed layer in June 1987 was 0.28
copopods L 1 (data of D. Mackas). These copeods were able to clear 0.15 ct 1 L, or
- 15% of the water column. In order to sustain their populations, the protozoons would
have to replace themselves at a rate of - 0.15 cfl. This rate is in general agreement with
the net ciliate growth rate of O. 10 d· 1 observed in the mesocosm experiments condueted
during June, 1987 (LANDRY, GIFFORD, KIRCHMAN, WHEELER and MONGER, 1993)
It is also consistent with FROST's (1993) revised model of the subaretic Pacific
ecosystem. Thus it appears that the grazing rates cf Neocalanus spp. on Protozoo
observed in this study are of appropriate magnitude to maintain the balance ot the
protozoan prey populations in the subaretic Pacific during Iate spring. Control cf
protozoan populations during other seasons is discussed by FROST (1993). A similar
calculation tor Ca/anus finmarchicus produces a similar resutt: Ca/anus abundance
in the upper water column was 0.85 L· 1 and 0.50 L· 1 in May and August respectively
(BATCHELDER, VanKEUREN, VALLAINCOURT and SWIFT, submitted). Making the
simplifying assumption that all Ca/anus life history stages clear water at similar mean
rates, tor per capita clearance rates of O. 19 and 0.15 L COpepodl cf1 in May and August,
the Ca/anus assemblage was able to clear 16% and 8%, respectively, of the euphotic.
zone. To sustain their populations, the protozoon community would have to replace itself
at rates cf 0.08 to 0.16 d· 1 • These rates are similar to those observed in the North
Pacific.
In summary, Neoca/anus plumchrus appears to be an indiscriminate omnivore in the
subarctic Pacific environment, as suggested by FROST (1987), consuming micro-sized
( > 20lJm) phytoplankton and Protozoo with equal efficiency, obtaining on the order ot
80% of its nutrition fram Protozoo. Ca/anus finmarchicus is equally indiscriminate in
the high Iatitude North Atlantic environment. However, because phytoplankton stocks are
higher and large phytoplankton cells are more abundant in the North Atlantic than in the
NOrth Pacific, C. finmarchicus obtains a greater fraction of its daily ration from
chlorophyll.
Acknowledegments - Many thanks to tOO captains and crews cf RV T. G. Thompson and RV
Endeavor for facilitating the sea-going work in the North Paclfie and the North Atlantle. I thank
colleagues In tOO SUPER and ML-ML programs for generously sharlng data, time. and ldeas. Special
thanks to C.B. MUter, B.W. Frost, B.C. Booth. H.P. Batehelder, J. Marra and M.J. Perry. and to E.J.
Lessard for provtdlng data on the carbon eontent of heterotrophie dlnoflagellates prior to pubUcation.
J.E. Rabalals asslsted wlth sampie proeessing and data analysis In the North Paclfle. P.R. Garrahan,
E. Martln and L. Fessenden contrlbuted to efforts in the North Atlantle. The National SClenee
Foundatlon (OCE8613892) supported fleld work In the North Paclflc. The U.S. OffIce of Naval Research
(NOO014-J-1437) supported fieldwork In the North Atlantlc as weil as manuscrlpt productlon and the
authors' travel to the 1993 ICES meeting.
10
•
•
.
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~
"
,
.
~
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14
Table 1. Initial experimental conditions.
N. plumchrus
North Pacific
June, 1987
C. finmarchicus
North Atlantic
May, 1991
oe
8.4
C. finmarchicus
North Atlantic
August, 1991
oe
oe
Mixed layer temperature
7.0
Chlorophyll
0.4 P9L·l
0.90 P9l:
1345-5039 L· l
2058-2269 L· l
5023-5405 L· l
Copepod Iife
history stage
CV
CV
ev
Incubatlon volume
2.0 L
1.0 L
1.0 L
Number coppods bottle·1
2
10
15
Incubation duratlon
24 h
24 h
24 h
erotozoa
12.8
l
1.39 P9L·l
eTable 2. Mean feeding rates on Protozoa.
North Atlantlc
May, 1991
North Paclflc
June, 1987
North Atlantlc
August, 1991
Clearance rate
(mi copepod· l h· l )
22.7
7.8
6.2
Ingestion rate
(J.1gC copepod· 1 d·1)
3.7-12.8
0.9
2.6
15
Figure 1. Components of copepod diet.
N. plumehrus
C. Jinmarchicus
C. Jinmarchicus
1.00
-SS
0.75
c...
0
c0 0.50
~
CJ
f
~
0.25
North PaciCic
June,1987
North Atlantic North Atlantic
May, 1991
August, 1991
IEZ22J Phytoplankton 0
Protozoa