l MARINE ECOLOGY PROGRESS SERIES Vol. 134: 247-263, 1996 Published April 25 Mar Ecol Prog Ser l
Food web interactions in the plankton of Long Island bays, with preliminary observations on brown tide effects
Darcy J. Lonsdale*, Elizabeth M. Cosper, Woong-Seo Kim**,Michael Doall, Asha Divadeenam, Sigrun H. Jonasdottir*"
Marine Sciences Research Center, State University of New York at Stony Brook, Stony Brook,New York 11794-5000,USA
ABSTRACT We examined the relat~veImportance of phytoplankton and ciliates as prey for metazoan zooplankton and the role of predation in regulating ciliate populat~onsIn 2 Long Island (USA) bays Depth-integrated primary production (mg C m h-') was dominated by nannoplankton <5 pm In d~am- eter throughout the year, ranging from >95" of total production in mid-summer to an average of about 60%, in winter and early spnng Predator exclusion and addition experiments conducted in microcosms showed that the mortality coeff~cientof cil~ates(d.') from zooplankton predation was higher when larger phytoplankton (>l0 pm) contributed less to total primary productivity For adult copepods an Increase In the percentage ciliate contribution compdred to phytoplankton contnbution to total carbon Intake also coinc~dedwith the higher prrcrntages of small microdlgal production Egg production rates of Acartia spp were positively correlated to the net growth coefficient of cili~ites In contrast, mlcro- metazoa routinely obtalned >70% of th~~rtotal carbon ratlon from phytoplankton, and at times dunng spnng and summer, removed 23 to 52' 0 of the total depth-~ntegratedprlmary production In addit~on to protozoa, we suggest that microinetazoa part~cularlycopepod nauplii, may serve as a trophlc llnk between phytoplankton and mesozooplankton In Long Island bays
KEY WORDS. Zooplankton grazing and production Primary production Ciliates
INTRODUCTION 1991, Peconlc Bays In Bruno et a1 1983, Cospel et a1 1989) showed that nannoplankton was the major con- Tempol-a1 and spatial changes in phytoplankton tr~butorto planktonic prlmary production In summel abundance and composit~on reflect the dynamic Such sh~ftsIn the composit~onand slze structure of the nature of both physical and biological factors which phytoplankton community can have Important effects contribute to the growth and loss of cells (reviewed in on the fecundity and surv~vorshlpof zooplankton For Frost 1980). In Long Island bays (New York, USA), example, Kleppel (1992, Kleppel et a1 1991) has ques- diatoms are an important component of the late winter honed the role of dlatoms as optimal food for adult bloom, and are succeeded by smaller chrysophytes copepods in several locations (e g Acartia tonsa of the and chlorophytes in the summer months (Lively et al. Cal~forniacoast), a hypothesis that has been supported 1983). Investigations of primary productivity in these recently In Long Island Sound stud~es(Jonasdottlr bays (Great South Bay reviewed in Carpenter et al. 1994, Jonasdottlr et a1 1995) D~atomsmay also be an lnferlor food source compared to an~malprey for some meroplankton (e g decapod larvae Harms 1992) Exu- 'E-mail dlonsdale@ccmail sunysb edu dates from diatoms In a stationary growth phase may Present addresses actually ~nhlb~tcopepod glazing (Male] & Harris 1993) "Korean Ocean Research and Development Institute, PO Box 29, Seoul 425-600, Korea Clliates, dinoflagellates and other protlsts may provide "'Danlsh Inst~tutefor F~sherlesand Marlne Research, Char- a better nutnt~onalsource to fuel copepod egg produc- lottenlund Castle, DK-2920 C:harlottenlund, Denmark tlon compared to dlatoms because of chemical dlffer-
0 Inter-Research 1996 Resale of full artlcle not permitted 248 Mar Ecol Prog Ser 134: 247-263, 1996
ences in speciflc fatty aclds and protein content bioactive compound that reduces gill ciliary beat fre- (Stoecker & Capuzzo 1990 and references therein, quency in some b~valvespecies (e.g Mercenaria mer- Jonasdottir 1994) cenaria; Gainey & Shumway 1991). The purpose of our study was to clvdluate the relative importance of phytoplankton and ciliates in feeding and production of metazoan zooplankton in 2 Long METHODS Island bays. In recent years, the importance of protists, particularily phagotrophic ciliates and flagellates, in Field sampling. Our sampling sites during 1991 maintaining the coupling of phytoplankton produc- included 1 station (Blue Point on 2/12, 3/21, 4/16, 5/2, tivity to zooplankton dynamics has become evident 7/25, 7/31, 11/25; dates expressed as month/day) in the (Conover 1982, Landry & Lehner-Fournier 1988, Sherr Great South Bay (GSB) and 2 stations in the Peconic et al. 1988). Because smaller algae, particularly those Bays (PB) (Reeves Bay on 5/20, 5/21, and West Neck <5 pm, are more likely to be efficiently utilized by pro- Bay on 6/17, 6/20, 7/17, 7/22) (Fig. 1). Both primary tozoa compared to adult copepods (Azam et al. 1983), productivity and zooplankton feeding experiments we hypothesized that predation on ciliates would be were conducted on each experimental date except on critical for copepod diets (as found for Acarfia tonsa; 5/2, 5/20, 6/20 when only the former was measured. Robertson 1983, Gifford & Dagg 1991) and production Sampling was conducted from piers or docks at a 0.5 m (Stoecker & Egloff 1987, reviewed in Stoecker & depth for temperature and salinity measurements, zoo- Capuzzo 1990), especially during summer when small plankton abundance, and ambient seawater collection. nannoplankton dominate in Long Island bays. The Strong vertical mixing of these shallow water bodies specific objectives of this study were, firstly, to deter- over large areas alleviated the necessity for water col- mine if there was seasonal variation in major food umn depth profiles (Bruno et al. 1983, Lively et al. resources for mesozooplankton (>202 pm) and micro- 1983). metazoa (>64 to 202 pm) in Long Island Bays. Sec- Zooplankton composition and abundance. Larger ondly, we investigated whether prey productivity zooplankton were collected and size fractionated by influenced copepod productivity. Thirdly, we evalu- success~velypasslng buckets of water (20 1) through ated the role of zooplankton predators on the popula- Nitex sieves; 202 pm and 64 pm for mesozooplankton tion dynamics of ciliates. During the course of this and micrometazoa, respectively (n = 2 for each size investigation a 'brown tide' occurred. This algal spe- fraction). Animals caught on the sieves were rinsed cies, Aureococcus anophagefferens, is -2 pm in diam- with 0.22 pm filtered seawater into jars, preserved in eter (Sieburth et al. 1988), and has toxic properties that 5% buffered formalin and enumerated under a dis- cause growth and feeding reduction in some marine secting microscope. Additional samples of whole sea- organisms (e.g. bay scallop larvae; Gallager et al. water (400 ml, n = 2) were collected and preserved in 1989). Dimethylsulfoniopropionate (DMSP), a precur- Lugol's fixative (-10%) for enumeration of more deli- sor to dimethylsu.lfide (DMS) and acrylic acid, resides cate ciliates. Lugol's samples were allowed to settle for within the cell (Keller et al. 1989). The cell surface of -48 h in the sa.mpling jar, followed by removal of 300 to A. anophagefferens contains a neurotransmittor-like, 350 m1 of the overlying water. The remaining contents
Fig. 1. Location of sampling s~tesin the Peconic Bays (RB: Reeves Bay; WNB: West Neck Bay) and Great South Bay (BP: Blue Point) Lonsdale et a1 : Planktonic interactions 249
were then placed in a graduated cylinder, and allowed for inoculations with radioactive sodium bicarbonate. to settle for an additional 24 h. All but 5 m1 of the over- These cultures were maintained under the same lying water was removed and protozoa were counted growth conditions as the stock cultures for 48 h prior to by 1 m1 aliquots in a counting chamber until at least the experiment to ensure uniform radioactive labeling 100 ciliates were counted. A Zeiss compound micro- of cells. scope equipped with a micrometer was used for enu- Seawater for the grazing experiments was collected meration and measurement of ciliates >20 pm. by bucket, placed into 20 l cubltainers, and transported Primary productivity and phytoplankton biomass. to and held in the laboratory in coolers to maintain Phytoplankton biomass was estimated from 90% ace- ambient temperature. Sampling was conducted in the tone-extracted chlorophyll a (chl a) by fluorometry morning, most often between 07:OO and 10,00 h. Gi-az- using a Turner designs fluorometer (Strickland & Par- ing experiments generally began within 3 h after sea- sons 1972, Cosper et al. 1989).Ambient seawater sam- water collection. All experiments were conducted at ples (30 ml) were size fractionated to obtain <5,
for cell-size dependent differences in radiolabeling same meth0d.s described above, incl.uding being (Tackx & Daro 1993). counted in 1 m1 aliquots of settled sample in a counting To account for radiolabel uptake by zooplankton not chamber until at least 100 individuals were counted. related to grazing (e.g. naupliar 'drinking'; Tester & The net growth coefficient of ciliates (d-l), zooplank- Turner 1991), controls were conducted using the same ton predation coefficient (or mortality coefficient of cil- amount of radiolabeled suspension as in the grazing iate~;d-l), and zooplankton predation rate (ciliates experiments, but first passed through a 0.22 pm Milli- ind.-' d-l) were calculated using the equations of Frost pore filter, and then added to grazing chambers as (1972). Some error in the estimation of zooplankton above. Filtrate controls (n = 2) were conducted for ea.ch predation may have occurred, however, if the net microalgal tracer and experimental date. A second growth coefficient of ciliates in the sieved treatment series of controls was conducted once to determine to did not match that in WSW. Carbon ingestion rates what extent radiolabeled cells were retained succes- from ciliate prey were estimated by vo1ume:carbon sively on 202 pm and 64 pm sieves. Grazing chambers relationships for tint~nnids (Verity & Langdon 1984) containing ambient filtered seawater (0.45 pm) were and aloricate ciliates (Putt & Stoecker 1989). Aloricate inoculated with algal suspension at 5 representative ciliates (n = 5 on each date) were assumed to be ball concentrations (cells ml-l; n = 4 to 12 for each concen- shaped, and the diameter (d) of the cell was measured tration), followed by size-fractionated sieving, and and its volume assumed to be equal to 4/3rr(d/2)3.Tintin- scintillation counting (see Lonsdale & Cosper 1994). nids (n = 5) were assumed to approximate a cylinder Zooplankton clearance rates were calculated from and thus both the length (l) and diameter of the lorica control-corrected data. Carbon ingestion rates (pg C were measured and the volume of a cell was estimated ind.-' h-') of the 4 size fractions of phytoplankton were by rr(d,i)21.Although zooplankton clearance rates (m1 calculated from clearance rates (m1 ind.-' h-') and ind. ' d-') were calculated for the total ciliate popula- phytoplankton carbon concentration (pg C I-'). Total tion, carbon ingestion rates were calculated separately carbon ingestion rate was determined from summation from grazlng rates on each ciliate type, and then of the ingestion rates of the 4 size fractions. In several totaled. cases, no phytoplankton biomass was measured but Adults and nauplii of the abundant copepod species minimal primary production was detected. Thus, car- were sorted from cod-end, 64 pm net hauls to provide bon ingestion rates were obtained from zooplankton additional information on the predatory impact of clearance and primary productivity rates (yg C I-' h-'). mesozooplankton and micrometazoa, respectively, on Zooplankton predation and population growth of population growth of ciliates. Ten adults or 50 nauplii ciliates. Estimates of mesozooplankton and micro- were added to 2 l polycarbonate bottles containing metazoan predation on ciliates were obtained using a unfiltered seawater (n = 2 for each copepod treatment). predator removal/addition method. Incubation bottles Before belng added to bottles, individual copepods (2 l polycarbonate bottles) were filled with whole sea- were transferred 3 times to 0.22 pm filtered seawater water (WSW) or size-fractionated seawater to remove with a pipet to minimize the introduction of other the >202 or al.l>64 pm zooplankton predators (n = 2 for plankton. Sampling protocols and incubation condi- each treatment). The latter treatment was used to esti- t~onswere as described for predator removal studies. mate the net growth coefficient of ciliates 164 pm (d-'; Zooplankton predation coefficients were calculated sensu Frost 1972. Stoecker et al. 1983), and the other using the realized ciliate growth coefficient calculated treatments to assess the predatory impact on ciliates of from WS\V incubations, rather than the net growth all larger (>64 pm) zooplankton (WSW control mea- coefficient as in the removal experiments. sured the realized rate of ciliate population increase), Copepod egg production and hatching success. To or only the micrornetazoa (>64 to 202 pm; >202 pm determine if egg production rates of the most common removal treatment). We use the term 'net growth' to copepods were food-limited (sensu Durbin et al. 1983), describe ciliate production available to larger zoo- or influenced by prey availability, 5 to 6 females of the plankton, recognizing that cannibalism or parasitism most common species [i.e. Acartia hudsonica(Piley) may occur (e.g. Stoecker et al. 1983). Bottles were and Acartia tonsa Dana] were put into each of 8 to 12 incubated for about 24 h outdoors in water tanks at plexiglass cylinders with a 202 pm Nitex mesh on the 40% natural sunlight by using neutral density screen- lower end, and hung inside 1 1 beakers. The 202 pm ing. Water temperature was maintained close to ambi- mesh in the inner containers allowed eggs to pass ent with ice and/or running tap water. Initial microzoo- through, and kept females separate to minimize egg pl.ankton samples (400 ml, n = 2; Lugol's preserved) cannibalism. Half the beakers were filled with 800 m1 were taken from treatment and control waters, and of 64 pm screened ambient water, and the remaining again at the termination of the experiment for each with 800 m1 of enriched, screened ambient water. The incubation bottle. Ciliates were counted using th.e screening was needed to remove any copepod eggs Lonsdale et al.: Plan~ktonic interactions 25 1
and nauplii present in the water. Enrichment consisted airtight white plastic box. Distilled water In the bottom of adding the flagellate Rhodomonas lens (7 to 8 pm of the box served to reduce evaporation from the wells. diameter) to achieve a minimum of 2.0 X 104 cells ml-l. Observations on copepod survival and molting were This nlicroalgal species has been found to be a good made twice daily. All of the copepod growth suspension food source for Acartia spp., and the experimental was replaced during the day, and 50 % was replaced at density is above the critical concentration for growth night. Observations were made for 4.5 d. Percentage (Jonasdottir 1994). Beakers were incubated at ambient survival was calculated from the number of individuals temperatures (usually ?l°C) in dim light on a 14:lO h surviving from NI to C I for Coullana canadensis and 1ight:dark cycle. Egg production rates under ambient N V1 to C 111 for Acartia hudsonica, and included those food conditions were determined after 24 h. Copepods surviving to the end of the experimental period if the fi- in the enriched beakers were allowed to acclimate to nal developmental stage had not been reached. Devel- the new food for 24 h. Following acclimation, the water opment times (h) used in the data analyses were from was screened again through a 64 pm mesh to remove only those copepods which reached either C1 (C. eggs and nauplii, and animals were placed back in the canadensis) or C 111 (A. hudsonica). same enriched water for another 24 h incubation. All Statistical analyses. Prior to analysis of variance and eggs and nauplii were counted, and eggs were placed multiple regression, Bartlett's test or the F,,,,, test was in culture plate wells (20 ml) to determine egg hatch- used to verify that variances around the mean, includ- ing success (%). Eggs were observed once a day for 2 ing those of transformed data, were homogeneous to 4 d to measure hatching success. Hatching success (Sokal & Rohlf 1981; pc statistical package). For multi- for eggs produced under ambient food conditions was ple regression, a sample size of 1 was included in the always determined, but not until 5/21 for eggs pro- data set (Sokal & Rohlf 1981). Statistical analyses were duced under enriched conditions. Percentage hatching conducted using either SAS (Analysis of Variance) or of eggs under ambient conditions was not available on the pc statistical package accompanying Sokal & Rohlf 7/17 because of their inadvertent loss following (1981; Linear Regression, Multiple Regression, Tukey- counting. Kramer procedure and R X C Test of Independence). Copepod development and survival with brown tide. To evaluate further how Aureococcus anophagef- ferens impacts the growth of copepods, NI to NI1 RESULTS nauplii of the meroplanktonic harpacticoid Coullana canadensis and mostly N V1 of Acartia hudsonica were Primary productivity rates and biomass taken from laboratory batch cultures maintained at 20°C and 16"C, respectively, a salinity of 25%0 and The highest rates of depth-integrated primary pro- under a 14:lO h 1ight:dark cycle (see Lonsdale & Lev- duction (Fig. 2) were measured in the summer months, inton 1985 for detail). A. hudsonica is common in Long and this can be attributed to increasing water temper- Island bays from winter through late spring (e.g. Great ature (Fig. 3). A multiple regression of the dependence South Bay; Duguay et al. 1989, this study), while C. of total primary productivity (mg C m-2 h-2, log,,,trans- canadensis nauplii have been found in summer (e.g. formed) on water temperature ("C) and total chl a Quantuck Creek on the south shore; Lonsdale et al. showed only water temperature to be significantly 1993). related (df = 1,10, F = 20.436, p < 0.001 and F = 1.156, Five food treatments were utilized; ambient (non- p > 0.25, respectively). The model explained 67.6% of bloom) seawater (26%0,sieved through 44 pm mesh the variance and was significant at the 0.005 level (df = netting) or ambient-enriched with either a bloom con- 2,10, F = 10.426).The major contributor to the total centration of Aureococcus anophagefferens (5 X 105 depth-integrated rate of primary production on all cells ml-l) or Thalassiosira pseudonana (3H) (1.22 X sampling dates was phytoplankton <5 pm in diameter. 105 cells ml-l). Both additions were equivalent to The range of contribution of these small phytoplankton 1100 1-19 C 1-' according to the equations of Strathmann to the total primary production was 45.8 to 95.7%, (1967). Alternatively, copepods were reared in auto- being greatest in the summer months and lowest dur- claved, filtered (20 pm) seawater (25L), with or with- ing winter and spring. The next-largest size fraction out a suspension of A. anophagefferens cells (5 X 105 (5 to 10 pm) contributed nominally to phytoplankton cells ml-l). Water temperature and the light cycle were community productivity (range = 0 to 6.7 %). The con- the same as for batch culturing of copepods. The vari- tribution to primary production by the larger phyto- ous copepod growth media were prepared fresh daily. plankton (>l0 pm) ranged from 5 to 47.9 %, and in gen- Nauplii and copepodites (n = 18 for each food treat- eral was greatest between February and early May. ment and life stage) were placed individually in 1 m1 Chl a concentration had a similar trend as found for wells of a multi-depression dish contained within an primary productivity (Fig. 4). The 5 pm fraction was 252 Mar Ecol Prog Ser 134: 247-263, 1996
350 Fig. 2. Depth-~ntegratedrate of primary productivity of 4 size fract~onsof phytoplankton in (A)Great South 300 Bay, (B) Peconlc Bays. Total depth-integrated rate of primary productivity is represented by the entire bar 2% 7E 200 o! ton, and the pennate diatom Cylindrotheca E 0 clostenum was the most abundant component of the >20 pm size fraction. A few Gymno- VF' loo dinium spp. were also noted. During the early g 50 spring (3/21),the >20 pm size fraction was com- z> posed of the centric diatoms Coscinodiscus sp. ',m fib MX Apr May JU~ JUI AU~sep erNOV ~kt U (-70 to 100 pm), Rhizosolenia setigera, and Rhi- o zosolenia sp., and the dinoflagellates Prorocen- & 140 U trum sp., Gymnodinium spp., and Protopen- L IZO dinium bipes. e 0 loo Lc f 80 Zooplankton abundances Q 60 P Late-stage copepodites and adult copepods, primarily Acartia spp. (A, hudsonica from Feb- 40 ruary through May, and A, tonsa in June and 20 July), comprised most of the mesozooplankton size fraction (>202 pm; Fig. 6).The micrometa- 0
San F& bar AT May Jun JUI AU~ SC~ &L Nov DCC zoan slze fraction (>64 pm to 202 pm) was com- Month
0 always the major component, ranging from 50 to 251 99.3% of the total phytoplankton biomass. Chl a 0 On concentration also was related to water temperature G 0 0 (linear regression; logl0y= 0.853 +0.015x; df = 1,49,
F = 10.321, 0.001 < p < 0.005). 15- e A bloom of Aureococcus anophagefferens oc- 0 0 curred in West Neck Bay of the Peconic Bays system during June and July, and reached a peak concen- &' tration of 1.43 x 106 cells ml-' on 6/17 (Fig. 5). By 5- 7/22, the bloom had dissipated, and the concentra- q 0 tion of this picoplankter was only 2.74 X 104 cells Jan Feb Mar Ap May Jun Jul Aug Sep 0.3 Nov ml-l. Dinoflagellates were also abundant during the brown tide peak, including Dinophysis acuminata (30 to 40 pm, 'red tide'), Gymnodinium spp. (>20 pm, 'red tide'), and Polykrikos kofoidi (60 to 80 pm, a heterotrophic dinoflagellate). During the decline of the brown tide (7/22), Gymnodinium spp. (220 pm) and Protoperidinium sp. (220 pm, a het- erotroph) were noted. In GSB during the same sum- mer period (7/25), a Nannochloris-like sp. (chloro- phyte -2 pm in diameter) was the major component of the <5 pm size fraction of planktonic phytoplank-
Dec Fig. 3. (A) Water temperature and (B) salinity in Great Jan Feb Mar Apr May Jun Jul Aug Sep 0.3 Nov South Bay (GSB) and the Peconic Bays (PB) Month : Lonsdale et al.:Planktonic interactions
Fig. 4. Chlorophyll a concentration of 4 size fractions of phytoplankton In (A) Great South Bay. (B)Peconic Bays. Total chl a concentration is represented by the entire bar 50
40 represented by tintinnids and aloricate ciliates. 30 F- The latter group were primarily oligotrichs in 0)5 20 the family Strombidiidae. Scuticociliates were Y also frequently found. Following the decline of c 'O =o the brown tide in PB (7/22), however, the pop- o ulation was composed almost exclusively of Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec C small (-30 to 40 pm), aloricate ciliates at a den- Q, 0 sity >20000 I-'. 0C 70 60 -0 Population dynamics of ciliates
40 Multiple regression analysis revealed that the net growth coefficient of ciliate populations 30 (d-';Fig. 8) determined from grazer removal 20 experiments was significantly correlated with water temperature (Table 2). Net growth coef- 10 ficients were positive througho'ut the sampling
o period except in February in GSB when water Jan Feb Mar Apr May Jun Jul Aug Sep Oct NOV Dec temperature was the lowest (2.5OC),and dur- Month ing the peak of brown tide in PB (6/17). The highest rate of population increase was 1.24 d-' prised mostly of copepod nauplii and meroplanktonic in PB during May. This analysis also showed a signifi- larvae (Fig. 6, Table 1) except on 7/25 and 7/31 when cant negative effect of cell concentration of Aureococ- large tintinnids were also abundant. The mean density cus anophagefferens on ciliate population growth. of total metazoan zooplankton was substantially lower Salinity (%o)and total and 8/17 7/10 7/21 8 8/20 '/U 6/27 'I2 7.6 7/17 7/22 Date Date Fig. 5. Concentration of Aureococcus anophagefferens in Fig. 6. Abundance (mean + range, n = 2) of mesozooplankton West Neck Bay, PB during 1991 Dates glven as Month/Day and micrometazoa 254 Mar Ecol Prog Ser 134 247-263, 1996 Table 1. Abundance (number 1-l)of the most common zoo- hS9 Whole seawater plankton taxa >64 to 202 pm in Great South Bay (GSB] and - m ) 64 pm zooplankton removed the Peconic Bays (PB) during 1991 Taxon Date (MonthlDay) 2/12 3/21 4/16 7/25 7/31 11/25 GSB Copepod nauphi 83.5 48.1 617.8 423.8 163.5 31.1 Polychaete larvae 0.0 0.0 38.8 35.8 8.5 0.2 Barnacle larvae 0.0 0.0 1.8 1.0 0.0 0.0 Tintinnids 0.2 0.0 0.0 236.0 110.5 0.8 5/20 6/17 7/17 7/22 PB ---- =B------PE------cSB---- Copepod nauplii 49.5 14.2 19.9 18.0 Polychaetc! larvae 3.4 0.3 0.6 4.2 Date Barnacle 1al\dc, 57.4 1.3 0.0 0.1 Fig. 8. Per capita rate of change (mean * range, n = 2) of cili- Tintinnlds 0.2 0.0 0.0 0.0 ate populations determined in microcosm experiments. The net growth coefficient of the ciliate population is shown as the >64 pm zooplankton removal treatment Table 2. Dependence of the net growth coefficient of ciliate populations (d.') on ambient physical factors (*Cand *h),pri- mary productivity (mg C m-L h-'), and brown tide concentra- hZ9 All zooplankton predators ) 64 pm tion (X 105 cells ml-l) in Long Island bays determined from O Micrometazoan predators multiple regression analysis. The model was significant (df = 2.0 5,14,F= 15.047; p < 0.001), and explained 68.0'K of the vari- p ance In the net growth coefficient I Wa .a 10 C Variable Partial regression F P .d0) v coefficient (df = 1,14) 'C.d 0.0 Intercept 0 807 0 Temperature 0 077 10 914 O.O05 Table 3. Dependence of the mortality coeff~cientof ciliates ulation growth. The average mortality coefficient of (d l) on water temperature ("C),total zooplankton abundance ciliates due to micrometazoa was on average 67.8% of (number I-'),primary productivity C m-2 h-'), tide the tota] mortality from all zooplankton. There was no concentration (X 105 cells m].'), and the initial concentration of clllates (numberl-l, determined frommultiple significant difference among the mortality coefficients analysis. The model was signifi.cant (df = 6,13; F= 7 496; 0.001 from the 2 zooplankton treatments (t-test for paired p < 0.005), and explained 77 6%) of the vanance in the comparisons of mortality coefficients on each date; df = mortality coefficient 19, t = 1.23, 0.2 p < 0.4). Val-]able Part~alregression F P coefficient (dI = 1,13) Zooplankton grazing and predation Intercept 1.535 Temperature -0.062 5.591 0.025 Table 5. Carbon ingested (pg C ind:' h-'; mean I 1 SE, n = 4) by mesozooplankton (M)and micrometazoa (m)from 4 size frac- tions of the phytoplankton comn~unity.Total carbon ingestion does not always equalthe summation of all fractions due to round- ing errors. Radioiabeled, laboratory cultured microalgae were used as tracers of size-selective grazing; <5 pm diameter: Nan- ~OC~~O~JSsp.; 5-10 pm: Thalassiorsira pseudonana; 10-20 pm: Thalassiosira weissflog~i,>20 pm: Ditylum brightwelli. Negative ~ngestionrates are shown as 0. Brown tide dates in West Neck Bay,Peconic Bays system are noted by ' Date Phytoplankton size-fraction (pm diameter) < 5 5-10 10-20 S 20 Total 2/12 M 0.026 (0.012) 0.009 (0.003) 0.004 (0.005) 0.005 (0.003) 0.043 m 0.005 (0.003) 0.002 (0.003) 0.003 (0,001) <0.001 (0.003) 0.011 3/21 M 1.339 (0.293) 0.075 (0.027) 0.030 (0.010) 0.005 (0.006) 1.449 m 0.067 (0.017) 0.004 (<0.001) 0.003 (<0.001) 0.001 (<0.001) 0.075 4/16 M 0.023 (0.017) 0.009 (0.008) 0.017 (0.010) 0.011 (0.007) 0.060 m 0.024 (0.024) <0.001 (<0.001) 0.017 (0.011) 0.009 (0.005) 0.051 5/21 M 0.002 (0,001) 0 0.004 (0.002) 0 0.007 m <0.001 [<0.001) 0 <0.001 (<0.001) 0 <0.001 '6/17 M 0 0 <0.001 (<0.001.) 0 <0.001 m 0 <0.001 ( with Thalassiosira pseudonana as a tracer on 3/21 and addition experiments, naupliar clearance rates on cili- 458.7 m1 ind.-' d-l with Nannochloris sp. on 7/22). On ates were positive for only 50% of the experimental only 1 sampling date (7/22) was the clearance rate on dates (Fig. 10). Clearance rates of micrometazoa were ciliates less than that on phytoplankton for adult cope- not effected by prey type (paired t-test; df = 9, t = pods. For micrometazoa, however, the dietary impor- 0.910, p > 0.2). tance of the larger ciliates is less certain. In the grazer Copepod egg production and hatching Table 6. Total carbon ingested (pg C ind:' h-') (I)and percentage carbon success intake from phytoplankton (PP) and ciliates (C) for totalmesozooplankton and rnicrometazoa Copepod egg production during summer (i.e, by Acartia tonsa) was limited by food, Bay Date Mesozooplankton Micrometazoa but this was not true in winter or spring (i.e. I PP C I PP C by A. hudsonica; Fig. 12).This was shown by GSB 2/12 0 041 92.1 7.2 0.011 97 6 2.4 the significant effect of sampling date X food 3/2 1 1.451 99.9 0.1 0.075 99 4 0.6 treatment (ambient or enriched) on egg pro- 4/16 0.085 70.7 29.3 0.051 100.0 0.0 duction rate [log(number + 1) female-' d-'; 2-way ANOVA; df = 6,48, F = 4.74, p < 0.0011. Egg production rate also increased significantly during the summer (df = 6,48, F = 60.44, p < 0.0001 for sampling date effect; df = 1,48, F = 2.29, p = 0.14 for food GSB 7/25 0.071 10.1 7/3 1 0.037 32.7 treatment effect). 11/25 0.550 87.5 Under ambient food conditions, water tem- perature did not correlate with egg produc- Lonsdale et al.: Planktonic interactions Table 7. Total depth-integrated carbon lngested (mg C m-' - m Mesozooplankton h ') (I)and percentage of total depth-integrated primary pro- 4 I Micrometazoa duction consumed by mesozooplankton and micrometazoa U Bay Date Mesozooplankton Micrometazoa I % I %> I GSB 2/12 2.638 14.9 2.197 12.4 3/2 1 6.086 24.5 5.627 22.6 4/16 4.952 5.1 50.371 52.3 GSB 7/25 6.529 3.9 7/31 4.525 1.4 Date 11/25 12.524 29.5 Fig. 11. Average clearance rate (*l SE, generally, n = 16 for all size fraction clearance rates) of mesozooplankton and micro- metazoa on the total phytoplankton community tion rate (Multiple Regression analysis; Table 8). How- ever, the production of ciliate food resources, as mea- data sets were not normally distributed with an arcsine sured by their net growth coefficient, was directly re- transformation, and thus a non-parametric test was lated to copepod reproduction. The cell concentration necessary; Sokal & Rohlf 1981). The lowest success of Aureococcus anophagefferens was negatively corre- occurred during the winter months. lated to egg production rate, and likely reflected the fact that ciliate growth and A. anophagefferens cell concentration were negatively correlated (Table 2). All Copepod development rate and survival remaining environmental variables, including copepod with brown tide species and total and > 10 pm depth-integrated primary productivity, did not correlate to egg production rate. Naupliar and copepodite survival were not affected Egg hatching success of copepod eggs produced by the addition of either Thalassiosira pseudonana or under ambient food conditions remained high brown tide cells to ambient seawater compared to throughout the study (> 75 %; Fig. 13), although there ambient conditions. Survival of copepods with only was an effect of sampling date (RX C test of indepen- brown tide cells for food was the same as in autoclaved dence, df = 5, G = 50.081, p > 0.001. Variances in the seawater (Fig. 14). In suspension of only brown tide ES3Adult copepod h Copepod naupl~us Ambient l O Micrornetazoa D Enriched -0 125 i l - 0 ------PE------=B ---- Date Date Fig. 10. Clearance rate (mean t range, n = 2) of zooplankton Fig. 12. Mean egg production rate (*l SE, n = 3 to 6) of Acar- predators (copepod adults, copepod nauplii, and natural tia spp. under ambient and enriched food conditions. Experi- assemblages of micrometazoa) on ciliates 264 pm ments were not conducted on 6/17, 7/22 or 11/25 MarEcol Prog Ser 134: 247-263, 1996 Table 8. Dependence of ambi.ent egg production rate (log 6S¶ Ambient number + 1 copepod-' d-') on water temperature ("C), cope- O Enriched pod species composition, primary productivity (mg C m-2 h-'), brown tide concentration (X 10' cells ml-l), and the net growth coefficient of ciliates (d") determined from multiple regres- sion analysis. The model was significant (df = 6.27; F= 28.660; p < 0.001) and explained 86.4% of the variance in egg pro- duction rate Vanable Partial regression F I coefficient (df = 1,27) Intercept 0.521 Temperature 0.047 0.633 0 25 Table 9. Mean (?l SE) development tim.e (h) of Acartia hud- sonica copepodites (C1to CIII) and Coullana canadensis nau- plii (NI to Cl) reared und.er 3 food, treatments (AMB: ambient seawater; AMB + 3H: ambient seawater enriched with Tha- Iassiosira pseudonana cells; and AMB+ BT: ambient sea- water enriched with Aureococcus anophagefferens cells). Copepods did not complete development with only filtered seawater or brown tide cells Species Treatment AMB AMB+3H AMB+BT A. hudsonica n 8 10 12 X 67.5 61.3 72.7 SE 3.3 1.5 5.5 C. canadensjs n 13 14 X 112.1 116.2 SE 1.8 1.7 cells or filtered seawater, nauplii and copepodites did not molt past NI1 or CII, respectively. Copepodite development rates were not significantly different among the 3 other food treatments (ambient, ambient + brown tide cells, amb~ent+ T pseudonana cells; l-way ANOVA,df = 2,27,F= 1.33, p = 0.28;Table g), but nau- pliar development rate was faster with 3H additions compared to ambient or brown tide addition treat- ments (ANOVA, df = 2,39, F = 10.95, p = 0.0002, and Fig. 14. Percentage survival of laboratory-reared copepods. Tukey-Kramer unplanned comparisons among means (A) Acartia hudsonica (NVI to CIII] and (B] Coullana at 0.05 level of significance). Thus, the brown tide did canadensis (NI to Cl), reared under 16 and 20°C, respec- tively, and 5 food treatments (BT: brown tide cells only; not contribute to or hinder growth and survival of FSW: filtered seawater; A: ambient seawater; A + BT: ambient copepods at lower bloom concentrations (i.e. 5 X 105 plus brown tide cels; A + 3H: ambient plus Thalassiosira cells ml-') in the presence of alternate food sources. pseudonand cells) Lonsdale et al.: Pla~nktonic interactions 259 DISCUSSION micrometazoa on natural plankton desplte the fact that their weight-specific ingestion rates may be 3 to 4 This study supports the idea that predation on proto- times higher than adults, and that numerically they are zoa is critical for copepod production in summer when usually very important (e.g. Lonsdale & Coull 1977, nannoplankton <5 pm dominate the phytoplankton. Turner 1982). Using other I4C tracer techniques (i.e. Although larger nannoplankton and netplankton Daro 1978, Roman & Rublee 1981), Kim (1993) found (>20 pm) never dominated the plankton in terms of that the micrometazoan community in the Peconic either productivity or biomass, phytoplankton was a Bays system graze on average 0.3 to 10.0% of total major source of carbon nutrition for copepods in winter depth-integrated primary productivity compared with and spring. Holoplanktonic and rneroplanktonlc lar- 0.2 to 4.3% for mesozooplankton. In GSB in summer, vae, however, almost always utilized phytoplankton to we found that micrometazoa consume the greatest per- obtain the majority of their carbon ration. The carbon centage of total depth-integrated primary productivity ration accrued from ciliates by micrometazoa may be a compared to mesozooplankton (Table 6). The impact of passive consequence of feeding on phytoplankton as micrometazoan grazing was greatest when copepod no prey-dependent difference in clearance rates was nauplii were an abundant taxon (i.e. 4/16 and 7/25; found. In contrast, adult copepods routinely had a Table 1). Thus, these results agree with studies in the higher clearance rate on ciliates compared to phyto- Chesapeake Bay (White & Roman 1992b) that showed plankton throughout the year. copepod nauplii often accounted for a large proportion Laboratory studies by Jonsson & Tiselius (1990) of the total zooplankton grazing, and removed up to showed that Acartia tonsa adults switched between 50% of the total depth-integrated primary production suspension and raptorial feeding depending on the in summer. concentration of phytoplankton. Acartia spent more Zooplankton predation on a major nannoplankton time in suspension feeding under high concentrations consumer, the ciliates (Capriulo & Carpenter 1980, of the flagellate Rhodomonas balfica (-8 pm width, Verity 1985, Sherr et al. 1991, Pierce & Turner 1992 13 pm length) compared to low or moderate concentra- and references therein, Turner & Granell 1992), may tions. Such a switch in feeding behavior could explain contribute to the dominance of small phytoplankton in our field results which indicated that the mortality GSB, particularly in summer (Kim 1993). And although coefficient of ciliates from all zooplankton was not specifically studied herein, we propose that meso- inversely correlated with >l0 pm primary productivity zooplankton predatio:n on micrometazoa, especially and positively related to total depth-integrated pri- copepod nauplii (Lonsdale et al. 1979), could at times mary productivity (Fig. 9, Table 2). Necessary for this also have a 'cascading' (sensu Carpenter et al. 1987) explanation would be the lack of response (detection?) influence on the phytoplankton community. We have by copepods to the high productivity rates of the <5 pm shown herein that micrornetazoa are important grazers phytoplankton in summer, and hence raptorial feeding of phytoplankton in Long Island bays, and it is known may predominate. However, a concomitant increase that copepod nauplii are prey for some adult copepods in adult copepod clearance rates (per individual) on (e.g. Landry 1981). Thus, copepod nauplii likely serve ciliates in the summer was not obvious in our study as an additional link between primary productivity and (Fig. 10), except during the peak of the brown tide. mesozooplankton productivity in Long Island bays. As Increased ciliate concentrations during the summer an example, depending on naupliar species and stage, may have negated the necessity for increased time adult Acartia tonsa may consume between 1.4 to 8.4 spent in raptorial feeding for copepods to increase nauplii d-' at a concentration ranging from -50 to 300 their ration. prey 1-' (Lonsdale et al. 1979). Thus, it is possible that Our finding that in GSB in summer, ciliates were mesozooplankton could obtain up to an additional more important than phytoplankton in mesozooplank- 0.015 1-19 C ind.-' h-' from copepod nauplii, which is ton diets does not match studies in Chesapeake Bay. about 11 to 29% of that obtained from ciliate predation For Acartia tonsa, at least, over 80% of the carbon in summer (i.e. 7/25 and 7/31). [We used the dry ingested was from phytoplankton in August compared weight of Acartia clausi NV and NVI, 0.1 pg (Marshal1 to only 19% in May in Chesapeake Bay (White & 1973), and assumed a carbon equivalent of 41.6% of Roman 1992a). These differences could be due to vari- the dry weight (Beers 1966) to estimate naupliar car- ation among locations in the composition of phyto- bon content.] Naupliar predation by mesozooplankton plankton, although a seasonal shift from diatoms to fla- may also be an important trophic link between primary gellates is also characteristic of Chesapeake Bay prod.uctivity and copepod productivity in the Chesa- (Malone et al. 1988, cited by White & Roman 1992b). peake Bay because nauplii also consume a significant Few studies have measured feeding rates of mero- fraction of the primary productivity (White & Roman planktonic and holoplanktonic larvae and other 1992b). Mar Ecol Prog Ser 134: 247-263, 1996 Our grazing experiments were conducted for 7 min ingestion rates of ciliates in Long Island bays match to minl~llize error from carbon recycling processes. closely that found by Gifford & Dagg (1991); average = Extrapolation of these short-term experiments to daily 0.4 pg C ind.-l d-' in winterhpring, and 2.5 pg C id-' rates may not be appropriate given that zooplankton d.' in summedfall compared with 0.1 and 2.1 pg C can exhibit die1 variation in grazing activity. Roman et copepod-' d-l, respectively, for A. tonsa in Louisiana. al. (1988) found that coastal copepods often showed Mesozooplankton were found to have high inges- higher feeding at night and that oceanic forms some- tion rates on phytoplankton in the spring in Long times had higher feeding rates during the day. Meso- Island bays and copepod egg production was not food zooplankton clearance rates on phytoplankton that we limited, at least as measured by our food enrichment measured using radiolabeled algae were similar to studies. Over the course of spring and summer, how- Louisiana (USA) field populations of Acartia tonsa ever, we found that egg production was not related to determined from gut pigment analysis (Gifford & Dagg either total or >l0 pm depth-integrated primary pro- 1991) when the exceptionally high mean for 3/21 duction, but to the net growth coefficient of ciliates. In (155.2 m1 ind.-' d-'; Fig. 11) is excluded from the data Chesapeake Bay following the spring bloom, egg pro- set [yearly average on all algal species = 3.4 (k1.9 duction by Acartia tonsa was also positively related to 95% CI) m1 ind.-' d-l compared to 3.6 m1 ind.-' d-l, microzooplankton (> 10 pm) (measured as carbon con- respectively]. Including the 3/21 clearance rate data centration), while no re1ati.on.shi.p to chl a concentra- also resulted in no significant difference among the tion (total or >l0 pm size fraction) was found despite studies (18.6 + 29.8 95% CI). Also, total carbon in- substantial ingestion of phytoplankton (White & gestion rates of phytoplankton had similar seasonally Roman 1992a). based trends. For Long Island bays, ingestion rates There have been numerous field studies that con- averaged 0.9 pg C ind.-' d-' in summer (i.e. primarily clude that water temperature is a major factor control- A. tonsa) and 9.8 yg C ind.-' d-' in wintedspring (A. ling egg production rate in copepods (e.g. Durbin et al. hudsonica), and in Louisiana, 1.9 and 4.7 pg C cope- 1992). Our result showing no relationship of copepod pod-' d-', respectively (A. tonsa year-round). Limita- egg production to temperature is not particularly tions of the radiotracer technique for measuring zoo- strong because we have Limited data for each copepod plankton grazing, however, became apparent during species (i.e. Acartia hudsonica and A. tonsa). However, the experiments conducted in PB during the brown a significant positive effect of temperature on egg pro- tide. The negative clearance rates of micrometazoa on duction rate was calculated when the net growth rate <5 pm microalgae at this time are attributed to an of ciliates was not included as an independent variable experimental artifact due to the large number of Nan- in the multiple regression analysis (df = 1,28, F = nochloris sp, tracer cells retained on the 64 pm sieve 18.080, p < 0.001). White & Roman (1992a) found that at the high experimental concentrations (20% of the both water temperature and carbon concentration of <5 pm biomass; Lonsdale & Cosper 1994) that masked microzooplankton, and not phytoplankton abundance, any detectable feeding by the few micrometazoa (16.5 were 'the best indicators of A. tonsa reproductive to 23.7 I-'). Occassionally, relatively high values for the potential in Chesapeake Bay'. Perhaps the correlation filtrate control were also obtained, and we can only between water temperature and egg production rate speculate as to the cause. Variation in grazing rate esti- found in some field studies may partially reflect the mates within a sampling date was likely due to varia- underlying relationship of water temperature effects tion in zooplankton density in the grazing chambers, on the production rate of ciliate populations (Table 2). especially when density was low (e.g on 3/21 when th.e average mesozooplankton concentration was low- est, 2.8 I-'). Ciliate population dynamics In Long Island bays, mesozooplankton clearance rates on ciliates when Acartia tonsa was abundant Robertson (1983) suggested that tintinnid population were mostly comparable to other studies of copepods growth would only be suppressed when adult copepod preying on natural assemblages of ciliates and/or other densities exceeded 10 1-' (also see Pierce & Turner protists such as Euglenoid sp. (average = 25.2 and 1992). In GSB, at least, adult copepod populations rou- 23.8 m1 copepod-' d-'; Gifford & Dagg 1991, Kim & tinely exceeded this concentration, ranging from 2.8 to Chang 1992, respectively). The clearance rates on cili- 248 1-' (Fig. 6). Ciliate population growth, however, ates in Long Island bays when A. hudsonica was dom- was also suppressed by micrometazoa predation that inant, however, were on average higher than those in a contributed on average 67.8 % to the total daily mortal- natural prey assemblage during a dinoflagellate bloom ity from all zooplankton. This substantial influence on in another temperate bay (4.8 to 9.6 m1 copepod d-'; ciliate population growth was found despite the fact Turner & Anderson 1983). Mesozooplankton carbon that ciliates contributed only a small percentage, usu- Lonsdale et al.: Plankton~cinterilctlons 26 1 ally <30%, to the daily carbon ration of micrometazoa. 1989),and abundances were not unlike those we found It is possible, however, that our measures of ciliate during the 1991 non-bloom year For 1986, when mortality from predation deviated from nature. For extensive monitoring of the brown tide was conducted example, small-scale turbulence impacts the detection in GSB, the average concentration was 1.4 x 105 cells and/or contact rates of some predators and prey (e.g. ml-l, and reached a peak of only 6 to 7 x 105 cells ml-' Rothschlld & Osborn 1988),and turbulence effects may (Nuzzl & Waters 1989). Other phytoplankton such as have been altered in the microcosnls. A~annochlonssp., a likely food resource for many pro- The net growth coefficient of ciliatc populations that tozoa, also outnumbered A, anophagefferens. Thus, we measured in Long Island bays (Fiy. 8) was always microbial processes likely remalned intact, and lower than during spring in a Massachusetts bay; 1.55 allowed for normal levels of zooplankton productivity. and 0.77 d-' for an aloricate and large tintinnid, Durbin & Durbin (1989) also provide evidence that respectively (Stoecker et al. 1983). During the spring lower concentrations of brown tide cells are not espe- and summer in Long Island bays, however, the net cially detrimental to zooplankton production. They growth coefficient of aloricate ciliates reached 1.17 to reported that Acartia tonsa weight, 'condition factor', 1.31 d-' (7/22 and 5/20, respectively). Tintinnid growth and egg production rate during a brown tide (7.6 X 105 rates, on the other hand, reached a maximum rate of cells ml-l) in Narragansett Bay (Rhode Island, USA) only 0.35 d" found in early spring (3/21). were low, but not unlike those sometimes found in other non-bloom years. We found that egg production rates were significantly affected by the brown tide, but Brown tide effects on plankton trophic interactions this observation (?/l?) was made just after the 'brown tide had reached over 1 X 106cells n11-' on 7/14 (Fig. 5). This investigation shows the importance of ciliates in However, we cannot conclude from our limited sam- the diets of metazoan zooplankton, and provides pling in 1991 that the lower summer density of PB zoo- insight into the manner in which blooms of Aureococ- plankton compared to GSB was due to brown tide cell cus anophagefferens may alter plankton dynamics. concentration on 6/17 because these differences may Previous studies on plankton dynamics in Long Island be due to local differences, and we do not have esti- bays during brown tides have shown that grazing, mates for West Neck Bay (PB) prior to the bloom. measured with fluorescently labeled algae and bacte- ria, and growth of some specles of protozoa were not suppressed in the presence of a brown tide (PB and Conclusion GSB;Caron et al. 1989), yet we found ciliate popula- tion growth to be negatively affected. It is noteworthy This study has shown that the relative importance of that the cell concentrations of A. anophagefferens phytoplankton and ciliates as prey differs among under which Caron et al. conducted their laboratory mesozooplankton and micrometazoa in Long Island and field investigations were lower (1 X 106 cells ml-' bays. But, because their food resource niches are not and -1 X 104 to 4 X 105 cells ml-l, respectively) than mutually exclusive, and because micrometazoa com- during our study on 6/17 (1.46 X 106 cells ml-l) when a prise a major component all larger zooplankton, negative growth rate of the ciliate population occurred exploitative competition for ciliates is likely intense, (Fig. 8). We also found that the density of aloricate cili- particularly in the summer During summer, the mor- ates increased substantially from 6/17 to 7/22 (230 to tality coefficient often exceeds the net growth coeffi- 27400 1-') d.uring the decline of the brown tide (to 3 X cient of ciliates, and thus ciliates may be in short sup- 104 cells ml-l). Thus, these 2 studies are not inconsis- ply. The effects of competition for cillates may be tent, but rather suggest a 'threshold' phenomenon in especially acute for mesozooplankton, and this hypoth- which microbial processes, especially protozoan graz- esis is supported by our finding that ambient food ing and production, continue over a wide range of cell resources limited the production rate of copepod eggs concentrations of A. anophagefferens,and are disrup- during the summer months. We do not have similar ted only during peak bloom conditions (i.e. >l X 106 evidence to determine the impact of food limitation on cells ml-l). This hypothesis is further supported by our growth of micrometazoa. However, it is probable that laboratory findings on copepod growth and survival, food limitation effects under non-bloom conditions which showed that at 5 X 10"ells ml-' there were no would be minimal on copepod naupliar or polychaete detrimental effects of the bl-own tide if alternate food larval growth, as also found for ciliates, because phyto- sources were available. plankton is not in short supply, at least as measured by During 1985 and 1986, the bloom of Aureococcus rates of prlmary productivity in Long Island bays. anophagefferens did not appear to be associated with Future studies on the role of food limitation on zoo- reduced copepod abundances in GSB (Duguay et al. plankton growth and survival rates will provide insight Mar Ecol Prog 5er 134: 247-263, 1996 Into the biological processes controlling recruitment In Duguay LE, Monteleone DM, Quaylietta C (1989) Abundance coastal bays. Measurements of food limitation in roo- and distribution of zooplankton and ichthyoplankton in plankton will also enhance our understanding of the Great South Bay, New York during the brown tide out- breaks of 1985 and 1986. In: Cosper EM, Bricel] VM, Car- evolution and significance of life-history variation penter EJ (eds) Novel phytoplankton blooms: causes and among marine invertebrate populations. impacts of recurrent brown tides and other unusual blooms. Lecture notes on coastal and estuarine studies. Springer-Verlag. Berlin, p 599-623 Acknowledgements. This research was funded by the New Durbin AG. Durbin EG (1989) Effect of the 'brown tide' on York State Living Manne Resources Institute and New York feeding, size and egg laying rate of adult female Acartia State Sea Grant College. Phytoplankton identifications were tonsa. In: Cosper EM, Bricelj VM, Carpenter EJ (eds) made by Dr Man Chang (Visiting Scholar from the Korean Novel phytoplankton blooms: causes and impacts of recur- Ocean Research and Development Institu te). We appreciate rent brown tides and other unusual blooms. Lecture notes the manuscipt review by Dr Gordon Taylor (Marine Sc~ences on coaslal and estuarine studies. Spri:nyer-Verlag, Berlin, Research Center) and helpful comments of 3 anonymous p 625-645 reviewers. This is Contribution 1009 of the Marinc Sciences Durbin EG, Durbin AG, Campbell RG (1992) Body size and Research Center. egg production in the marine copepod Acartia hudsonica during a winter-spring bloom In Narragansett Bay. Llmnol Oceanogr 37:342-360 LITERATURE CITED Durbin EG, Durbin AG, Smayda TJ. Verity PG (1983) Food limitation of production by adult Acartia tonsa in Narra- Anderson DM, Kulis DM, Cetta CM, Cosper EM (1989) gansett Bay, Rhode Island. 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