effects of temperature and food abundance on …...limnol. oceanogr., 37(2), 1992, 36 l-378 0 1992,...

Limnol. Oceanogr., 37(2), 1992, 36 l-378 0 1992, by the American Society of Limnology and Oceanography, Inc.

Effects of temperature and food abundance on grazing and short-term weight change in the marine copepod Acartia hudsonica

Edward G. Durbin and Ann G. Durbin Graduate School of Oceanography, University of Rhode Island, Narragansett 02882- 1197

Abstract

Ingestion and short-term weight change in adult female Acartia hudsonica were investigated at 4.5”, 8”, 12”, and 16°C with the solitary diatom Thalassiosira constricta as food. Narragansett Bay copepods were preadapted to the desired temperature and saturating food level for 3 d to standardize feeding history before the experiments. Maximal ingestion rates at the four temperatures were 16,460, 14,120, 2 1,470, and 29,960 cells copepod-‘d-l or 43.9, 37.2, 67.9, and 92.9% body C (Q10 = 2.3) and 34.2, 30.7, 42.6, and 74.7% body N d-’ (Q10 = 2.4). The critical concentration varied between 840 and 1,900 cells ml-’ (0.17-0.23 pg C ml-l) and was not significantly related to temperature. Maximal clearance rate was similar at all temperatures (20.8-23.9 ml copepod-Id-l), but .on a weight-specific basis increased from 3.3 to 6.0 ml (pg copepod C)-‘d -I between 4.5” and 16°C (Q10 = 1.8). Feeding rates at 4.5” and 8°C were similar; the seemingly low ingestion rates at 8°C were interpreted as evidence for a senescent population of adult copepods in the bay from late April to early May.

During preadaptation at high food, A. hudsonica body C and N either stayed constant (indicating saturating food in the field) or increased (indicating food limitation in situ). Body weight was sensitive to variation in food supply; during the 24-h feeding experiments weight remained stable at the two highest food levels, but declined significantly at lower levels. Maximal observed weight loss was temperature-dependent, increasing from - 15% C and 12% N d-l at 4.5”C to 25% C and 17% N d-l at 16°C.

The relationship between temperature and feeding rate in marine copepods has seldom been investigated, although temperature effects on respiration, reproduction, growth and development, and gut evacuation are relatively well known (e.g. Mullin and Brooks 1970; Vidal 1980~; Dam and Pe- terson 1988; McLaren et al. 1989). Of par- ticular interest are the effects of temperature on the maximum rates of feeding (I,,,) and clearance (E,,,), and the food concentrations associated with the lower feeding threshold (C,) and the attainment of Imax (the critical concentration Cc), as these pa- rameters define the functional relationship between food abundance and feeding rate

Acknowledgments We thank Robert G. Campbell for assistance in the

field and laboratory work, Einar Hjorleifsson for advice concerning computer analysis of the data, R. Choudary Hanumara for statistical advice, Theodore J. Smayda for permission to use the C-N analyzer in his laboratory, and Marilyn Maley for assistance in manuscript preparation. We also thank three reviewers for their comments on the manuscript.

This research was supported by the Biological Oceanography Program of the National Science Foun- dation (OCE 82- 14836).

and are basic input for ecological models. The relation between temperature and feeding has been explored through compilations of data from various sources (e.g. Huntley and Boyd 1984), but the application of these generalized relationships to individual species is open to question (Lehman 1988). In the few studies of temperature effects on F max and Imax within individual copepod species, the Qlo values varied widely: 3.2 for F,,, (5”-15°C) in Acartia hudsonica (Dea- son 1980); 3.9 for Z,,, (lo-1 5°C) in Centro- pages hamatus (Kiorboe et al. 1982), vs. 5.5 for F,,, representing pooled data from many species (Conover and Huntley 1980). Tem- perature effects on C, and Cc are virtually unexplored, although Wlodarczyk ( 19 8 8) recently examined the relationship between temperature and lower feeding threshold in the marine copepod A. hudsonica.

The effects of temperature and food availability on short-term changes in body weight are also poorly known in copepods. Al- though it is commonly assumed that weight in the adult is constant, body weight in Acartia (and by implication other small copepods) responds quickly to short-term variation in food supply (Durbin et al. 198 3,

361

362 Durbin and Durbin

Table 1. Sampling date, temperature, and phytoplankton biomass (Chl a and C in pg liter-*) in Narragansett Bay and size and chemical composition (pg cell-‘) of Thalassiosira constricta used as foodi in the Acartia hudsonica feeding experiments. C estimated assuming C: Chl Q = 60 (I>urbin et al. 1975). --,=z--- -- ---

T. constricta Field

-- Cell size Temp. (“c) Chl a C Composition

--- P--P 1984 Field Exptl. -- Vol. Total >lOpm

Diam Total >lOpm C N C’:N --P bm’) Cm)

7 Feb 2.4 S 23.0 - 1,380 - 216 14 Mar 3.1 4 16.0 - 41.3 !i.2 2,683 17.2’ 960 - 170 35.7 4.8 2,642 17.2

17 Apr 6.8 8 6.7 3.5 402 210 153 32.9 4.7 1 May 9.1 8 2.3 1.4 2,654 17.1 138 84 149 32.1 4.6 2,675 17.2

15 May 11.4 12 4.2 2.9 252 174 148 29.4 ii.0 29 May 15.6 12 8.4 3.9 2,254 16.2 504 234 150 23.5 6.4 - -

5 Jun 15.1 16 10.8 2.7 648 162 137 21.5 6.4 12 Jun 18.4 16 10.1 4.6 2,202 16.1 606 276 141 31.0 4.6 2,258 16.6 -v-p-- --

1992; Durbin and Durbin 1989). Such weight change should be quantified for studies of copepod feeding and bioenergetics, in order to scale ingestion rate to units of body weight and to properly account for growth (and degrowth) in energy budgets.

The present study examines the effects of temperature and food abundance on feeding rate and short-term change in body C and N in A. hudsonica Pinhey. Seasonally acclimated adult females were collected from Narragansett Ray, Rhode Island, during the winter--spring diatom bloom. Experimen- tally determined values of <Yc are compared with p’hytoplankton biomass in the bay to indicate whether food availability limits ingestion in situ. This study is the first to examine temperature and food effects on both feeding and weight change in a marine copepod and forms part of a larger investi- gation of the ecology ofA. hudsonica in Nar- ragansett Bay, a productive, temperate estuary. Seasonal changes in body size and egg productioa of A. hudsonica (Durbin et al. 1992) and the effect of the annual temperature cycle on the pattern of maturation and the age distribution of the adult copepods (Durbin and Durbin 1992) were also investigated.

Met hods Experiments were carried out in Febru-

ary-June 19 84 with seasonally acclimated females collected from a station in the lower bay (station location and environmental data given by Durbin et al. 1992). Experimental

temperatures were adjusted to follow the vernal warming of the bay and were within 3” of the field temperature (Table 1; table 2 of Durbin et al. 1992:). The use of field- collected copepods ensured that interactive effects of temperature, copepod size, and thermal acclimation in the experiments were appropriate for the natural population. Zoo- plankton were collected by gentle, vertical hauls of a 250-pm mesh, 0.5-m plankton net and returned to the laboratory within 1 h. Care was taken to prevent thermal shock during transport and later sorting of copepods.

Copepods were preconditioned for 72 h at a high concentration of the experimental food alga, the solitary diatom Thalassiosira constricta (2,500 cells ml-’ in 0.45-pm filtered seawater), in order to provide a known feeding history prior to the experiments. Within a few hours after capture we sorted adult female A. hudsonica into 4-liter glass jars containing the preconditioning medium to which nutrients (F/50, with ammonium nitrate as the N source: Guillard and Ryther 1962) were added to ensure that the cells did not become nutrient depleted. Jars were attached, normal to the axis of rotation, to a I rpm plankton wheel enclosed in a clear acrylic box through which temperature- conditioned water was circulated; temperature control was + 0.1 “C. Experimental temperatures were 4”-5”, 8”, 12”, and 16°C (Table 1). Light was provided with “cool- white” fluorescent bulbs mounted above each plankton wheel; the photon flux den-

Acartia grazing and weight 363

sity was 16.3 PEinst mm2 s-l. The light-dark cycle was adjusted to follow nature.

Stock cultures of T. constricta were grown in medium F/2 (Guillard and Ryther 1962) under the same temperature and light/dark cycles as in the experiments. All cultures were used when in the log phase of growth.

Feeding rate was measured at T. constricta concentrations ranging from 40-270 (lower range) to 2,300-3,100 (upper range) cells ml-l, obtained by adding different amounts of culture to 0.45~pm filtered seawater. The corresponding C and N concentrations ranged from 0.008-0.065 to 0.35- 0.59 pg C ml-’ and 0.001-0.014 to 0.05- 0.11 pg N ml-l. Desired concentrations of T. constricta were made up shortly before the experiment and dispensed into replicate grazer and control jars. Extra media at each concentration were reserved for topping off the jars. Experiments were carried out in l- and 2-liter widemouth glass jars, the jar lids fitted with a liner made of 3-mm-thick, closed-cell polyethylene foam to provide a tight seal. The jar size at each food concentration was chosen so that changes in phytoplankton cell numbers due to grazing would be detectable yet would not deplete cells by more than -30%. In the 4.5”C experiments, 1 -liter jars were used for cell concentrations > 500 cells ml-l; 2-liter jars were used for lower concentrations. At the higher temperatures, 1 -liter jars were used for concentrations >800-1,000 cells ml-’ and 2-liter jars for lower concentrations.

Experiments were carried out for 24 h over the same phase of the diel feeding cycle: experiments were begun between 1100 and 1400 hours, during the midday mini- mum of feeding by A. hudsonica (Wlodar- czyk 1988); final samples were collected in the same order as the initial ones exactly 24 h later. About 1.5 h was needed for the initial setup and final sampling of the jars. Two grazer and two control jars were used for each food concentration in the experiments. Two experiments were conducted at each temperature.

After preconditioning, the copepods were concentrated and randomly sorted in groups of 30 into jars containing the desired concentration of T. constricta. Jars were filled to the top, sealed, and mixed by gently in-

verting several times. A subsample of 50 ml was removed for initial cell counts, the sample volume replaced with extra media of the appropriate concentration, and the jar re- sealed and placed on the plankton wheel.

Phytoplankton growth rate at each food concentration was measured in control jars without grazers. Ammonium nitrate (to a final concentration of 15 PM) was added to all jars to prevent possible differential growth of the phytoplankton in experimental and control jars due to NH3 excretion by zooplankton (Roman and Rublee 1980). Initial and final subsamples were collected from each jar to provide an estimate of phytoplankton growth rate at each food concentration. At the end of the experiment, three subsamples from the control jars were filtered onto precombusted 13-mm Gelman AE glass-fiber filters for determination of phytoplankton cell C and N.

After the 24-h incubation each jar was removed from the plankton wheel, gently mixed by inverting several times, and a 50- ml subsample withdrawn with a pipette and preserved with l-2 drops of Lugol’s solution for later cell counts. Contents were then poured through a 153~pm Nitex screen to recover the copepods, which were anesthe- tized in a solution of 0.58 g 3-aminobenzoic acid ethyl ester (MS-222) liter-’ in chilled, filtered seawater. Copepods were counted and the developmental stage verified, then briefly rinsed in deionized water, and transferred to a precombusted Al pan for a pooled measurement of final C and N content of the copepods in each jar (the small size of A. hudsonica precluded C and N determi- nations on single animals). Occasionally, adult males or C5 females were added in- advertently to the jars during the initial sorting procedure. They were counted with the adult females for the calculation of ingestion rate but were not included in the final weight measurement. Mortality during the experiments was low and never exceeded 1 dead copepod jar-‘. Dead animals were included in neither the grazing-rate calculations nor the weight measurements.

Cephalothorax length, condition factor (CF), and C and N content were determined on a subsample of the catch on the day of collection from the field (table 2 of Durbin


et al. 1,992) for comparison with the final body weight of the copepods in the grazing experiments. Because length was not measured on the experimental animals we cannot compute the final CF, which normalizes weight per unit of length. To provide a first- order comparison of CF in the laboratory studies with that in the field, however, we estimated CF from the mean initial cephalothorax length and the final C and N content as

CF = (aW)/L3

where TV is weight (pg), L is cephalothorax length (mm), and a is an arbitrary scaling factor to bring CF near unity (a = 0.2 and 0.8 for C and N, respectively).

Phytoplankton cell concentrations > 200 cells ml-’ were determined with a Coulter model ZM-Cl 000 Accucomp System particle counter. Five 2-ml subsamples were counted and the mean value used to cal- culate ingestion rate or phytoplankton cell growth. Concentrations i 200 cells ml-’ were enumerated with a Zeiss model D in- verted microscope, using settled volumes of 3-8 ml of media depending on initial cell concentration. Three subsamples were counted per sample and the mean value determined. C and N were determined with a Hewlett-Packard model 18 5B analyzer.

Copepod ingestion rate, volume swept clear, and the instantaneous growth rate of phytoplankton at each cell concentration were calculated according to the equations of Frost (1972). In our experiments, however, we measured the initial as well as the final cell concentrations in each jar, rather than using a pooled initial value determined on the stock culture prior to dispensing into the experimental jars. Thus each jar in our experiment provided an independent estimate of grazing or phytoplankton growth rate II

The relationship between ingestion and phytoplankton abundance was described by an Ivlev curve modified to include an x-intercept possibly different from zero, corresponding to a lower feeding threshold (Mc- Allister 1970; Wlodarczyk 1988):

I = I,,,U - expl-B(C - C,)l> (1)

where I is ingestion, C is the mean phytoplankton concentration during the ingestion measurement, and Imax: B, and Ct are fitted constants. The parameter Imax is the asymptotic maximal ingestion and B is related to the degree of curvature in the relationship. A positive value for Ct would indicate the presence of a threshold concentration below which copepods, stop feeding. In a rectilinear model the critical concentration Cc is readily defined as the intersection between the two straight lines representing the ascending and horizontal phases of the ingestion curve (Frost 1!)72), but the corresponding definition of Cc in a continuous, asymptotic function like an Ivlev curve is less obvious. For present purposes we define Cc at 90% of Imax.

Nonlinear curves we:re fitted with a nonlinear least-squares estimation procedure on nontransformed data (Procedure NLIN, DUD method of computation) from the Statistical Analysis System (SAS) Version 5, on PC. Regression palrameters were compared among temper,atures by pairwise t-tests (Sokal and Rohlf 198 1). Statistical significance levels are I’ < 0.05 throughout this study.

Results Phytoplankton composition and growth

rate- T. constricta formed single cells in culture and at the four temperatures ranged from 2,202 to 2,683 pm3 (16.1-l 7.2~pm ESD), 137 to 216 pg C cell-l, and 21.5 to 41.3 pg N cell-’ (Table 1). Cell size and C and N content declined with increasing ex- yperimental temperature, but the C : N ratio did not change significantly.

The growth rate of T. constricta during the ingestion measurements was strongly dependent on initial ceI1 concentration; with increasing cell concentration the instantaneous daily growth ra,te k increased from 0.0 to 0.5 d-l at 4” and 8°C and 0.2 to 0.5 d--l at 12” and 16°C (Fig. 1). This concentra tion-dependent growth was a response to dilution of the laboratory-grown culture with new, unconditioned media to obtain the desired range of cell concentration for the feeding experiments. The greater the dilu-


tion, the longer the lag phase before the cells resumed exponential growth and thus the lower the instantaneous daily growth rate during the experiment. Although this phe- nomenon is well known from phytoplankton physiological studies (Fogg 1965), it seems to be less widely recognized in the zooplankton literature, where controls are sometimes measured at only one food concentration. Phytoplankton growth rate k should be measured at each food concentration to correct ingestion rate properly for cell growth.

Temperature and ingestion -Ingestion increased asymptotically with increasing food concentration (Figs. 2, 3,4). Estimates of Imax at each temperature were in good agreement (Table 2). Replicate experiments at each temperature were pooled and the relationship between ingestion and food concentration calculated according to Eq. 1 (Table 3).

Between 4.5” and 16°C lmax increased from 16,460 to 29,960 cells copepod-‘d-l (Table 3). The maximal ingestion rate (Imax) of cells was slightly lower at 8°C than at 4.5OC, although the difference was not significant (Table 3). Imax increased significantly, however, at 12” and 16°C.

I,,,,, expressed as ,wg C or N copepod-’ d-l followed a similar trend with increasing temperature as ingestion of cells, but the proportional increase was not the same because phytoplankton C and N content declined with increasing temperature (Table 3). Maximum ingestion of C and N was significantly lower at 8°C than at 4.5”C (Table 3). The increased ingestion of cells as 12” and 16°C was partially offset by the lower C and N content of the cells. As a result, I max for C and N at 12°C was not significantly different than at 4.5”C (but was significantly higher than at 8OC). I,,, at 16°C was significantly higher than at all lower temperatures. Over the range of 4.5”-16”C, I max increased from 3.17 to 4.19 pg C d-1 and 0.63 to 0.91 pg N d-l (Table 3).

Ingestion was also computed as the percentage body C or N eaten per day (Fig. 4), based on the final body weights at the end of the feeding experiments. Between 4.5” and 16°C Imax increased from 43.9 to 92.2% body

0.6 1

0.5

t 0 .

0.4 0

0.3 l

i

4 * t 0.2

: 4 0.1 A

0.0 16°C I . I . I 1

0.6 -I

it- ’ I . I . 1 I

0.6

y 0.5

0.4 2

0.6

0.5 A ru

l

,i$y , . , . ;%, * 0 1000 2000 3000

Cells I ml

Fig. 1. Instantaneous daily growth rate (k) of the unicellular diatom Thalassiosira constricta in relation to mean cell concentration in the grazing experiments. First experiment-o; second experiment-A.

C and 34.2 to 74.7% body N d-l. Again calculated maximal ingestion rates were lower at 8°C than at 4.5”C, but the differences were nonsignificant (Table 3). Imax increased significantly, however, at 12” and 16’C.

Overall, I,,, values at 16°C were significantly higher than at all other temperatures, while I,,, at 12°C was significantly different from all other temperatures except for 4.5”C ingestion of C and N; Imax at 8” was non- significantly different from 4.5”C ingestion as cells, body C, and body N, but significantly lower than at 4.5”C in terms of ingested C and N (Table 3).

Fitting nonlinear regressions to describe the relationship between I,,, and temperature T (“C) yields


“0 1000 2000 3000 Cells I ml Cells I ml

Fig. 2. Rates of ingestion (cells copepod -I d-l) and clearance (F, ml d- ‘) by adult female Acartia hudsonica fed Thalassiosira constricta at four temperatures. Symbols as in Fig. 1.

Z,,,(%body C) = 24.4 exp(0.083 2) Qlo = 2.3 (2)

and

I,,,(‘%body N) = 17.1 exp(0.089 2) Qlo = 2.4. (3)

At all four temperatures the Ivlev ingestion curve had a positive x-intercept, indicating a lower feeding threshold (CJ ranging from 46 to 127 cells ml-l, or 9-20 pg C ml- l and 2-4 pg N ml- l (Figs. 2, 3,4; Table 3). The 95% confidence intervals for the 4.5” and 8”‘C intercepts included the origin (O,O), but the intercepts for the 12” and 16°C curves were significantly greater than zero. The lower thresholds were not significantly different from one another according to pair-

wise t-tests, suggesting that the lower feeding threshold does not change significantly with increasing temperature.

The critical concentration varied between 840 and 1,900 cells ml-’ (0.17-0.23 pg C ml-l) and was not significantly correlated with temperature (Table 4). The somewhat arbitrary definition of the critical concentration for an Ivlev curve affects the value of C’,; defining C, at, sa.y, 95% of I,,, would yield slightly higher values of 1,060-2,290 cells ml-l (0.21-0.29 PC ml-‘) but would not alter the apparent temperature indepen- dence of C,.

Clearance rates peaked at moderately low food concentration and declined at lower and higher concentrations (Fig. 2). The clearance curve was similar to that shown for Acartia tonsa by Kiorboe et al. (1985)

Acartia grazing and height 367

Fig. 3. Ingestion as in Fig. 1.

4.0 - 6 “C

l.O- /

0.1 0.2 0.3 0.4 0.5 0.6 Carbon, pg I ml

0.6

0.6

0.0 0 0.02 0.04 0.06 0.06 0.10 0.12

Nitrogen pg I ml

of C and N (pg copepod-l d-l) by Acartia hudsonica fed Thalassiosira constricta. Symbols

and Paffenhiifer and Stearns ( 1988) and indicates that the relationship between ingestion rate and food concentration is curvi- linear rather than rectilinear (in which case clearance rate should have been constant and maximal at food concentrations below C, and declined curvilinearly above Cc: Frost 197 5). Maximal clearance rates occurred well below the critical concentration (Fig. 2), indicating that copepods began to de- crease clearance rates while still under limiting food. At the critical concentration the clearance rate was roughly half of F,,, (Ta- ble 4). In absolute terms, maximal clearance rates were remarkably similar at all four temperatures [mean (range) = 22.6 (20.8- 23.9) ml copepod-l d-l: Table 41. Because of the declining copepod body size with increasing temperature, however, maximal clearance rates on a weight-specific basis in-

creased from 3.3 to 6.0 ml (pg copepod C)) ’ d-l between 4.5” and 16°C (Table 4) where

F,,,[ml (pg body C-l) d-l] = 2.5 exp(0.056 2) Q10 = 1.8. (4)

The cell concentration CFm,, at which the maximum clearance rate F,,, was reached varied between 245 and 5 15 cells ml-’ (0.044-0.063 pg C ml-l) and was not significantly different among the temperatures (Table 4).

Temperature, food level, and weight change- Copepod body size declined with vernal warming of the bay (see table 2 of Durbin et al. 1992 for all data, and Table 5 of this study for the subset pertaining to the ingestion measurements). Weight also changed in the laboratory during the acclimation period and the feeding experiments.

Weight change during the 3-d acclimation


L .% 80 =

p" 60 m"

0 0.1 0.2 0.3 0.4 0.5 0.6 0 0.020.04 0.060.06 0.100.12 Carbon pg I ml Nitrogen pg I ml

Fig. 4. Ingestion of C and N (% body C and N copepod-’ d ‘) by Acartia hvdsonicu fed Thalassiosira constricta. Symbols as in Fig. 1.

was estimated by difference between the mean weight on the day of capture and the mean final weight of copepods at the two highest food concentrations in the ingestion experiment (Table 5). Weights of copepods

Table 2. Feeding by Acartia hudsonica females on Thalassiosira constricta at four temperatures. Asymp- totic maximal ingestion rate (I,,,,,, cells copepod-’ d-l), computed according to Eq. 1 for replicate experiments at each temperature. Each curve contains 12-14 data points. --

1984 Temp.(%) Imn., + SE

7 Feb 5 17,240+2,300 14. Mar 4 17,220k 1,540 17 Apr 8 16,050&650 1 May 8 13,070~920

15 May 12 20,270+- 2,070 29 May 12 22,260+2,070

5; Jun 16 29,740+4,370 1;‘. Jun 16 29,980+: 1,120

at the two highest food concentrations were not significantly different in any of the experiments, justifying pooling the data to obtain an overall mean value for copepods after 96 h at high food: 72 h of preconditioning at 2,500 cells ml-l T. constricta, plus 24 h at the experimental food concentration in the ingestion measurement.

The amount of growth during preadap- tion varied among experiments. C content increased significantly during the preadaptation period in the first 8” and both 16°C experiments; N increased significantly only in the first 8°C experiment (P < 0.05 by the W:ilcoxon signed-rank:s test). C and N content did not change significantly during acclimation for the second 8” and the two 12°C experiments. Initial weight data were not available for the experiments at 4”-5”C, but measurements during the egg production study (Durbin et al. 1992) indicated that


Table 3. Feeding by Acartia hudsonica females on Thalassiosira constricta at four temperatures. Data from replicate experiments at each temperature were combined and the probability between daily ingestion rate (I) and food concentration (C) determined according to

Z = I,.,{ 1 - exp[-B(C - C,)]} where C and C, = cells ml-’ x 1O-3 for Z = cells copepod-’ d-‘, = pg C ml-’ for Z = pg C or % body C d-‘, and = pg N ml-’ for Z = pg N or % body N d-‘. Ingestion as a function of food concentration and experiment temperature (T, “C) was computed from all data, where

Z = A{ 1 - exp[-B(C - C,)]exp(DT)}.

Ingestion Temp.

WI I,,,,, -t SE or A f SE B + SE C, + SE D f SE fl m.

cells d-’

pg C d-’

% body C d-*

pg N d-’

% body N d-’

cells d-’ % body C d-’ % body N d-’

4.5 16,460f 1,150* 8 14,120+750*

12 21,47Ok1,500 16 29,960-t-2,060 4.5 3.17f0.28* 8 2.13k0.12

12 3.20+0.22* 16 4.19f0.29 4.5 43.9+4.7* 8 37.2f 1.7*

12 67.9f4.3 16 92.9f6.4 4.5 0.6310.05* 8 0.4610.02

12 0.58+0.05* 16 0.9 1 kO.09 4.5 34.2f3.4* 8 30.711.5*

12 42.6f2.8 16 74.7f7.5 All 11,910+880 All 25.322.1 All 21.2f 1.8

2.03kO.47 3.232 1.24 1.93f0.44 1.3OkO.24

10.39k3.06 21.6Ok8.69 12.98f2.96 9.26k 1.75

1 l-2824.18 14.45k4.14 13.00+2.79 10.7622.20 52.8 1 I!I 14.00

100.34f40.32 68.57zk 17.25 38.06k9.28 58.88zk20.13 80.49k25.66 69.182 14.61 41.06& 10.44

1.74-cO.21 12.21+ 1.56 52.12zk7.36

0.046f0.039 0.85 5 0.127kO.072 0.71 6 0.095 kO.036 0.88 7 0.121 kO.037 0.92 8 0.009-t0.009 0.79 9 0.020*0.011 0.70 10 0.014~0.005 0.88 11 0.017~0.005 0.92 12 0.008kO.011 0.70 13 0.007~0.013 0.82 14 0.012kO.005 0.89 15 0.015+0.005 0.89 16 o.o02t-0.002 0.82 17 0.004+0.002 0.70 18 0.002-1-0.001 0.86 19 0.003~0.001 0.88 20 0.002~0.002 0.72 21 0.003~0.003 0.78 22 0.002 fO.OO 1 0.89 23 0.003 kO.002 0.87 24 0.08O-tO.023 0.050+0.005 0.86 25 0.01 l-tO.004 0.079+0.006 0.87 26 0.002-1-0.001 0.07 I kO.006 0.83 27

* IIn.. values not significantly different from one another (P > 0.05).

weight remained stable during preadapta- for 48 h in natural plankton enriched with tion for the 4”-5°C ingestion experiments. 2,000 cells ml-* of T. constricta and 10,000

Weight change during preadaptation for cells ml- * of the chain-forming diatom Skel- the ingestion measurements was similar to etonema costatum. In these experiments, that in the egg production measurements body C and N after 48 h at excess food were (Table 5) where copepods were incubated usually comparable to that after 96 h in the

Table 4. Feeding by Acartia hudsonica on Thalassiosira constricta at four temperatures. Comparisons of F max, the maximal clearance rate, and C,,,,, the concentration of T. constricta at which F,,,,, is reached, with FCC, the clearance rate at the critical concentration and C,, the critical concentration (T. constricta concentration corresponding to 90% of I,,,,,). Calculated from Eq. 5-8 in Table 3-(l); calculated from Eq. 13-16 in Table 3-(2).

F InPI Gn.. FCC C

(ml [ml olg body (cells (ml [ml Cue body copepod-’ d-‘) C)-’ d-‘1 ml-l) &Cm1 ‘) copepod ’ d-‘) C) ’ d-‘1 (cells ml-l)

Temp. (“c) (1) (2) (1) (2) (1) (2) (1) Ocg %-‘) 4.5 22.4 3.3 245 0.044 12.6 1.9 1,180 0.21 8 20.8 3.5 370 0.036 15.1 2.0 840 0.17

12 23.9 5.4 380 0.050 15.0 3.2 1,290 0.19 16 23.3 6.0 515 0.063 14.2 3.7 1,900 0.23

Durbin and Durbin

ingestion experiments, indicating that at high levels of food weight stabilized within the first 48 h after collection of the copepods from the field. An exception was the first 8°C experiment, when weight continued to increase after 48 h.

During the ingestion experiments copepod body C and N changed significantly over 24 h (Fig. 5). C and N contents were highest at the two highest food concentrations and declined with decreasing food level-a trend closely resembling that of ingestion. Be- cause all copepods received the same preconditioning and were of similar size at the beginning of the experiment, it is apparent that significant body C and N were lost during 24 h at limiting food. Weight loss may have included both spawning of eggs and catabolism of body tissue, but these pro- cesses cannot be separated because we did not measure egg production during the ingestion experiments.

Body C and N at each food level were normalized to mean weights at the two highest food concentrations, in order to show relative weight loss (Fig. 6). The percentage loss of C was greater than of N, indicating both the spawning of lipid-rich eggs and the preferential utilization of C reserves to sup- port metabolism, “sparing” N under limiting food conditions. The percentage loss of body constituents over 24 h increased with increasing temperature, from - 15% body C and 12% body N at 4.5”C to 25% body C and 17% body N at 16°C (Table 6, Fig. 6).

Copepod weight in the second 8°C experiment did not conform to the pattern in the other experiments. Final body size did not differ significantly with food level and indeed remained unchanged from the initial size at the time of collection. Low weight and CF indicated that the copepods w.ere in poor physiological condition at that time (Durbin et al. 1992).

Changes in the estimated CF during the 24-h feeding experiments can be compared with CF of adult female A. hudsonica in Narragansett Bay, where carbon CF varied between 1.3 1 and 1.89, and nitrogen CF between 1.40 and 1.78 (Table 6; table 2 of Durbin et al. 1992). In both the field and laboratory maximal carbon CF declined with warming temperature, while maximal


A A A

l

4' . ' " * ' 0 1000 2000 3000

Cells I ml 0 1000 2000 3000

Cells / ml

Fig. 5. Final C and N content of adult female Acartia hudsonica in relation to mean food concentration during 24-h grazing experiments at four temperatures. Copepods had been preconditioned for 3 d at 2,500 cells Thalassiosira constricta ml-‘, then transferred to different food concentrations for the measurement of feeding rate. Symbols as in Fig. 1.

nitrogen CF did not change. In the feeding 8”Cexperimentsand -1.5 to 1.1-1.2(-0.3- experiments the decline in carbon CF from 0.4 units) at 12” and 16°C. Corresponding the highest to the lowest food level was from values for nitrogen CF at high and low levels - 1.8 to 1.5 (-0.3 units) in the 4.5” and first offood were - 1.6-1.8 to 1.4-1.6 (-0.2-0.3

Table 6. Estimated condition factor of adult female Acartia hudsonica at the end of the 24-h ingestion experiments, based on final body C and N, and the average initial cephalothorax length measured on a separate subsample of copepods on the day of collection from the field. Estimated condition factors are shown for the highest and lowest food concentrations to indicate the ranges at the different food levels. The initial CF of the field-collected copepods is shown for comparison.

1984 Exp. No. Exptl. temp.

0 Initial

Carbon CF Nitrogen CF

Final Final

High food LQW food Initial High food Low food

14 Feb 2 5 1.76 1.50 - 1.79 1.58 20 Mar 5 4 - 17 Apr ii 8 1.40 1.78 1.50 1.48 1.64 1.48 1 May 8 1.31 1.33 1.34 1.40 1.46 1.49

15 May 9 12 1.56 1.46 1.25 1.83 1.69 1.45 29 May 11 12 1.59 1.52 1.16 1.70 1.73 1.40

5 Jun 12 16 1.38 1.55 1.18 1.49 1.64 1.37 12 Jun 13 16 1.41 1.55 1.13 1.58 1.71 1.41


~~~~~-7: *i :;p..‘:i;;; :y (y[!

i$fq~I.f 0 1000 2000 3000 0 1000 2000 3oa10

Cells / ml Cells / ml

Fig. 6. Differences in final weight of Acartia hudsonim after 24 h at different concentrations of Thalassiosira constricta, expressed as a percentage of the mean final weight at the two highest fcod concentrations in each experiment. Curves fitted visually; symbols as in Fig. 1.

units) at all four temperatures. In the second 8°C experiment where weight did not change significantly, CF remained near its initially very 1.0~ level (carbon CF and nitrogen CF 1.3 and 1.4 respectively). Thus the change in CF occurring over 24 h in the ingestion experiments was similar to the seasonal range observed during the winter-spring period in Narragansett Bay.

Discussion Maximal ingestion rate-Feeding by A.

hudsonica on the chain-forming diatom S. costatum has been investigated at temperatures comparable to ours (Smayda 1973; Deason 1980; Verity and Smayda 1989). S. costatum cells are smaller (34-69 pg C and 5.4-IO.1 pg N cell-l: Deason 1980) than T. constricta cells, but the effective particle size is uncertain because of variation in chain

length. Smayda (1973) found maximal ingestion rates of 42 and 60 x lo3 cells d-l at 4’ and 10°C. His 4°C data were comparable to those of Verity and Smayda (1989), where I,,, at 5°C ranged between 33 and 50 x 1 O3 cells d- * (N 19-:3 5% body C d-l, using mean values of 30 pg C cell-’ and 5.2 pg C copepod-l). These figures compare with our estimates where Zmax := 44, 37,68, and 93% body C d-’ at 4.5”, 8”, 12”, and 16”C, equivalent to 14.1 x lo3 cells and 34% body N d--l at 4.5”C, increasing to 29.9 x lo3 cells and 75% body N d-” at 16°C. In contrast, Deason (1980) reported much higher (though variable) values, where I,,,,, between 5” and 15°C increased from 84 to 660% body C d-l at. 500 pg C liter-’ and from 42 to 250% body N d-l at 50 pg N liter-l. These high I,,,, values are difficult to evaluate, but may reflect variations in


chain length contributing to the variability in her experimental results and the fact that her maximal food concentrations were higher than in the present study.

In our study the Q10 for Z,,, as a percentage of body C and N d-’ (2.3 and 2.4 respectively) was similar to the Q10 for egg production per unit of body C and N (2.7 and 2.4, respectively: Durbin et al. 1992). Our Q10 of 1.9 for I,,, (cells d-l) compares well with Smayda’s (1973) value of 1.6 for A. hudsonica fed S. costatum. The Q, c) for Zmax (cells, % body C and % body N -d-l) calculated from Deason’s data yielded very high estimates ranging from 8 to 15, although because of the perhaps unrealisti- cally high I,,,,, these Qlo values may be open to question. Her Q10 for F,,, (3.2) was much lower and more similar to other published values than for the Qlo for I,,,. Kiorboe et al. (1982) obtained a Q10 of 3.9 for I,,, of C. hamatus between 1” and 15°C. From Pe- tipa (1966), Kremer and Nixon (1978) calculated a Q1 O of 3.3 for I,,,,, in Acartia clausi. However Zmax values in Petipa’s study are relatively low (3.9-6 5.6% wet wt over 4”- 25”C), possibly because ingestion was estimated indirectly from measurement of respiration rate, neglecting egg production.

Feeding thresholds -A lower feeding threshold, or reduced clearance rate at low plankton abundance, has previously been described from Acartia sp. (e.g. Reeve and Walter 1977; Deason 1980; Paffenhiifer and Stearns 1988; Jonsson and Tiselius 1990). Feeding thresholds are generally higher for natural particle spectra than for cultured algae, perhaps because natural food contains significant amounts of nonnutritive or oth- erwise unavailable C (Parsons et al. 1967; McAllister 1970). In the laboratory Cf was shown to be inversely related to particle size (Frost 1975).

In most of these studies, including the present one, the exact threshold concentration was not closely determined and it is unclear whether feeding stopped at low plankton concentration or continued at a reduced rate below the lower threshold, Wlodarczyk (1988) used measurements of gut pigments to investigate feeding by A. hudsonica females fed T. constricta at very low concentration, however, and confirmed the existence of thresholds below which the

copepods stopped feeding. Lower thresholds ranged from 11.6 to 30.5 pg C liter-’ between 4” and 16”C, with no significant relation between C, and temperature. These lower thresholds were similar to our estimates (9-20 pg C liter-‘: Table 3).

Critical concentration - Cc for ingestion did not change significantly with temperature. Present results together with those of Wlodarczyk ( 19 8 8) indicate that, while clearance and ingestion rates in A. hudsonica change significantly with temperature, the food concentrations associated with the lower feeding threshold (Cl), the critical concentration (Cc), and the concentration for maximal clearance rate (CF,,,) do not. Comparable studies of temperature effects in other copepods seem to be lacking, although C, has been shown to be inversely related to food particle size (Frost 1972; Berggreen et al. 1988) and positively related to body size (Mullin and Brooks 1976). Vi- da1 (1980a,b,c,d) found that in Calanuspa- cz$cus the critical food concentration for maximal growth rate, body size, and production rate increased with temperature, but he did not examine temperature effects on ingestion.

Experimentally determined estimates of Cc may be compared with field phytoplankton concentration to identify periods of re- source limitation (Mayzaud and Poulet 1978, but see Hassett and Landry 1983). In the present study where field-collected copepods were preadapted at high food, Cc reflects well-fed copepods. Total and > lopm C concentrations in Narragansett Bay varied greatly during the study period, but were usually 2 Cc (Fig. 7). These results sug- gested nonlimiting food conditions during most of the winter-spring period, in accord with the experimental study of egg laying and body size, where food limitation was found only in late spring and did not appear to be severe (Durbin et al. 1992).

Clearance rates- Clearance rate in Acar- tia increases with particle size (e.g. Bartram 1980; Stoecker and Sanders 1985; Berg- green et al. 1988) and is reduced for noxious species (Tomas and Deason 198 1; Uye and Takamatsu 1990) and for particles of low or no nutritional quality (detritus: Roman 1977; plastic beads: Wilson 1973; Dona- ghay and Small 1979; phytoplankton in poor


(J.---L----- ’ Feb Mar Apr May Jun

Fig. 7. Comparisons of the critical concentration (C,) for Acartia hudsonica fed Thalassiosira constricta at four temperatures (heavy lines) with total and > lo- km C concentrations in Narragansett Bay during winter-spring 1984. C concentrations estimated from Chl a, assurning C : Chl a = 60 (Durbin et al. 1975).

physiological condition: Cowles et al. 1988; Kiorboe 1989).

Here F,,, in A. hudsonica ranged from 20.8 to 23.9 ml copepod-l d-l and did not change significantly with temperature within the range of 4.5”-16°C. When normalized to the: body weight of the copepods, however, .F,,, increased from 3.3 to 6.0 ml (pg body C)-’ d-l between 4.5” and 16”C, for a Q10 of 1.8. Deason (1980) reported much higher values for F,,,,, [2.7, 7.8, and 9.4 ml (pg dry wt)-l d-l at 5”, lo”, and 15”C]. If we assume that C was -42.6% of dry weight in A. hudsonica (Durbin et al. 1992), Dea- son’s clearance rates are equivalent to 6.3, 18.3, and 22.0 ml (pg body C)-l d-l and Q10 for F,,,,, = 3.2. Conover and Huntley (1980) obtained a higher Q10 of 5.5 for the relationship between F,,,,, and temperature, based. on pooled measurements from various sources.

In the present study maximal clearance rate occurred over a narrow concentration range and at relatively low food concentration, ‘similar to curves described for A. tonsa fed unialgal cultures by Kisrboe et al. (198 5) and Paffenhofer and Stearns (1988). In contrast Deason (1980) reported that F,,, in A. hudsonica fed the chain-forming diatom S. costatum extended over a fairly broad range of ceIl1 concentrations.

Food quality and ingestion-Comparison of ingestion curves is affected by the changes in algal cell and copepod body size with temperature. For example the decline in cell size with increasing temperature might tend to inflate Zmax for cells (i.e. increase apparent Q,& because the copepods must filter more

particles to obtain the same amount of C or N. Ingestion rates as the percent body C or N, however, are corrected for differences in algal and copepod size and facilitate comparison across temperatures.

In our study mean daily growth rate of the cells varied with experimental cell concentration, but whether chemical composition (food quality) varied similarly is un- known, as chemical analyses were performed only on the highest experimental concentration. Studies with chLemostat-grown cells, in which chemical composition was varied by changing the dilution rate and degree of nutrient limitation, indicate that clearance rate in A. tonsa was higher for cells of higher N content and correspondingly higher growth rate (Cowles et al. 1988; Kiorboe 1989). These experiments are not directly comparable to our study because the chemostat cultures were all nutrient limited to some degree, and the differences in growth rates and chemical composition represented steady state adaptation to the limiting nutrient in the culture. In our experiments, different growth rates represent a lag phase in growth brought about by inoculation of cells into unconditioned media rather than by nutrient limitation. Cells were always nutrient replete and thLere is no a priori rea- son to suspect different chemical composition. Thus food-quality effects that have been observed in chemostat experiments are unlikely to have affected our results.

Similar ingestion rates at 4.5” and 8”C- The similarity in maximal ingestion rates at 4.5” and 8°C was surprising, and suggests that ingestion was either elevated at 4.5” or suppressed at 8°C. Replicate experiments at each temperature were in good agreement, indicating that the similarity between the 4.5” and 8°C data was real. Phytoplankton growth rates were similar in the 4.5” and 8°C experiments (Fig. l), indicating that the physiological condition of the phytoplankton at the two temperatures was comparable.

The first hypothesis, that the 8°C ingestion rates were normal and the 4.5”C rates were elevated, is supported indirectly by a comparison of the maximal ingestion rate in this study with maximal growth rate in A. hudsonica as estirnated from published

Acartia grazing and weight . 375

Table 7. Maximal daily ration (% body C d-l) of adult female Acartia hudsonica compared with estimated maximal daily growth rate of copcpodite stages Cl-C5. Dry weight data from preserved A. hudsonica collected at the same locality in 1976; weights corrected for estimated 29.5% weight loss in Formalin (Durbin and Durbin 1978). Development time (0, d) from egg to adult female as a function of temperature (T, “C) was estimated from several sources (Landry 1975a,b; Durbin and Durbin 1992) where D = 1,288 (T + 2.327)-*.4774, and duration of Cl-C5 = 0.3290 (Landry 1975b). Instantaneous daily growth rate in C assumed equal to that for dry weight. Gross growth efficiency (K,) = growth/ingestion; growth in weight and egg production of the adult female assumed equal to daily growth increment in Cl-C5 (Berggreen et al. 1988).

Temp. (SC)

4.5 8

12 16

Cl-C5 instantaneous

Dry wt old D daily wt C69 daily increment ingestion

Cl c59 Egg-C69 Cl-C59 (% d-‘) (% body C d-l) K,

0.86 6.71 75.4 25.2 8.2 43.9 0.19 0.78 5.93 40.9 13.7 14.9 37.2 0.40 0.69 5.04 25.2 8.4 23.6 67.9 0.35 0.60 4.15 17.5 5.9 33.1 92.9 0.36

information on the weights of different copepodite stages (Durbin and Durbin 1978) and estimates of development time based principally on A. clausi from the west coast of North America (Landry 1975a,b; Durbin and Durbin 1992). Combining the weight increment between copepodite stages C 1 and C5 female with the estimated maximal development rate at the different temperatures, we compute an instantaneous rate of daily weight increase (Table 7). Dividing this figure by the maximal ingestion rate of the adult females we obtain an estimate of gross growth efficiency K,, assuming that production by adult females as body tissue and eggs is equivalent to biomass production in Cl-C5 (Berggreen et al. 1988). The K, values for 8”, 12”, and 16°C were similar (0.40, 0.35, and 0.36), suggesting that the maximal ingestion rates were internally consistent with the body size and maximal development rates at those temperatures. These estimates of growth efficiency were similar to the values of K, = 0.39 for C and 0.40 for N reported for A. tonsa at 18°C by Kisrboe et al. (1985). The K1 value of 0.19 for A. hudsonica at 4.5”C was lower than that of the other three temperatures, however, suggesting that the ingestion rate was high relative to the estimated potential growth rate of copepodites at this temperature. Further work to establish the Qlo for ingestion and growth at temperatures 14°C is needed to resolve this question.

The second hypothesis, that the 4.5”C feeding rates were normal but the 8°C rates

were low, is supported by seasonal changes in A. hudsonica body size and egg production rate (Durbin and Durbin 1992; Durbin et al. 1992). Size frequency distributions indicated that during the 8°C ingestion experiments, the adult female population was dominated by autumn-hatched, overwin- tering copepods whose poor CF and low egg production rate indicated that they were either senescent or thermally stressed by the rapidly warming bay temperature. Low phytoplankton concentration in the field may have affected ingestion capabilities at 8°C but egg production measurements did not indicate food limitation in situ. A reduced rate of feeding would be consistent with a population dominated by senescent adults (Ikeda 1977). A shift to a younger adult age structure between 1 and 8 May was accompanied by significant increases in mean weight, CF, and egg production, although food level continued to be low.

The two interpretations of the 4.5” and 8°C feeding data are not mutually exclusive and may be operating simultaneously. No firm conclusions can be reached, although we believe that the available evidence fa- vors the second interpretation (that the 8°C ingestion measurements were abnormally low).

Short-term changes in C and N content - Weight changes during experimental incu- bations reflect the adequacy of present and prior feeding conditions. An increase in weight indicates improved feeding conditions, while weight loss usually indicates de-


clining food. Constant weight may mean either that food is in excess and weight is stable at a maximum or that copepods are in poor physiological condition and are un- able to gain weight even when food is plen- tiful. In the latter case weight remains constant or declines (Durbin et al. 1992; the second 8°C experiments in this study). The low CF of such copepods distinguishes them from healthy, nonfood-limited animals (Durbrn et al. 1983, 1992).

Weight changed significantly during the 24-h feeding experiments. The loss of body C at the lowest food level increased from - 15% at 4.5”C to 25% at 16°C while N loss increased from 12 to 17% over that temperature range. The greater loss of C than N was consistent with Mayzaud’s (1976) findings for starved Calanus finmarchicus (CV). His data for A. clausi (=A. hudsonica), where measurements of weight and chemical composition were made on mixed life history stages, were more difficult to inter- pret. Although significant weight losses occurred during starvation, it appeared that differential mortality, which selectively removed the smaller animals during the starvation period, confounded the temporal pattern, and the rate of change in chemical composition could not be determined.

In ithe present study somatic weight changes could not be distinguished from changes in egg biomass within the copepods. Both represent real changes in body mass; spawned eggs simply represent biomass that is gained, shed, and replaced, rather than stored in the body. In A. hudsonica! at 4°C - 33% of the weight loss during 7 cl at limiting food was due to spawning of eggs, indicating that the remainder was somatic weight respired to meet energy needs (Durbin et al. 1992). The partitioning of energy between gonad and soma may change with temperature; in the benthic copepods Acanthocyclops viridis and Macrocyclops albidus, the proportion of ingested energy di- rected\ toward reproduction increased with temperature at the expense of somatic growth and respiration rate (Laybourn-Par- ry et al. 1988).

In feeding or bioenergetics studies it is important to document growth (or degrowth) occurring during the course of the

experiments. Weight change will affect feeding or production estimates that are normalized to body mass. Estimation of weight from length is unreliable because of poten- tially large changes in weight per unit of length (Durbin et al. 1983) and seasonal changes in chemical composition (Durbin et al. 1992). The significance of short-term weight changes for energy budget calculations can be estimated from the detailed study of A. tonsa bioenergetics at 18°C by Kiorboe et al. (1985). In that study copepod body weight was estimated from length; possible short-term changes in weight were not taken into account. In the energy budget in their table 3, ingestion at the lowest food level (18.0% of I,,, at 92 rug C liter-‘) was strongly food limited and significant weight loss probably occurred. Our data at 16°C and 95 pg C liter-’ indicate a loss of 19.5% body C and 12.0% body N over 24 h, of which perhaps 67% was somatic and the remainder was spawned eggs (Durbin et al. 1992). These figures indicate that at the lowest food level of Kiorboe et al. (198 5), most of the respired C and excreted N was fueled by catabolism of body tissue rather than by ingested food as they assumed. The confu- sion of endogenous and exogenous C and N in the energy budget .may explain the relatively high assimilation efficiency found at the lowest food level.

Rapid fluctuation in body weight is probably typical of small copepods that, like Acartia, do not store large amounts of lipid and have high potential fecundity and growth rates that are dependent on current food supply (see also Dagg 1977). Even copepods that store energy to enable them to withstand prolonged periods of insufficient food, however, may exhibit short- term changes in body composition. For example Corner et al. (1976) reported that Calanus helgolandicus adult females lost 7.56% of their body N after :!4 h without food at 10°C. Because body size reflects both the physiological condition of the copepods and food availability before and during laboratory experiments, greater emphasis should be placed on direct measurements of copepod weight and condition factor in future studies.


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Submitted: 6 October 1988 Accep fed: 10 October 1990 Revised: I5 October 1991

effects of temperature and food abundance on …...limnol. oceanogr., 37(2), 1992, 36 l-378 0 1992,...

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