Temperature and laboratory feeding rates in Carcinusmaenas L. (Decapoda: Portunidae) larvae from hatching through metamorphosis

J. Exp. Mar. Biol. Ecol., 1986, Vol. 99, pp. 133-147 Elsevier

133

JEM 705

TEMPERATURE

AND LABORATORY

FEEDING RATES IN CARCZNUS

MAENAS L. (DECAPODA : PORTUNIDAE) THROUGH

LARVAE FROM HATCHING

METAMORPHOSIS’

RALPH R. DAWIRS

and ANDREAS DIETRICH

BiologiischeAnstalt Helgoland, Meeresstation. D-2192 Helgoland, Federal Republic of Germany

(Received 11 December 1985; revision received 21 March 1986; accepted 24 March 1986) Abstract: Larvae of Carcinus maenas L. were reared in the laboratory and temperature-dependent

stage durations of successive instars were examined at 12, 15, 18, and 25 “C. Feeding rates (FR), in numbers of newly hatched Artemia nauplii, biomass, and energy consumed by a single crab larva during 24 h, were measured daily through the moulting cycles of all larval stages at the four temperatures. Dry weight (DW) and elemental content of carbon (C), nitrogen (N) and hydrogen (H) were analysed in newly hatched (0 h) and l-day-old (24 h) Artemia nauplii at six temperatures (6, 9, 12, 15, 18, 25 “C). Due to a 24 h feeding regime, the temperature dependent “mean nutritive value” of newly hatched brine shrimp nauplii is defined, individual biomass (DW, C, N, H) and energy (Joule) 12 h after hatching. General figures in changing individual daily FR, and temperature-dependent peculiarities are discussed. The total amount of food ingested by successive larval instars increases exponentially, while the increasing cumulative quantity consumed by individual crab larvae on successive days of development is described by power functions. At higher temperatures significantly less absolute biomass and energy is consumed during the entire larval development. C. maenas megalops are the main energy consumers in larval life, contributing 41 to 67% (12 to 25 “C) to the total larval energy intake between hatching and metamorphosis. Larval ability to adapt to increasing metabolic costs for maintenance in higher water temperatures is discussed with average daily feeding rates (AFR). Improved efficiencies are presented for the cumulative larval energy budget, 31% in assimilation, and 4.4% in gross growth (K,). Key words: Carcinus maenas; larval development; feeding rates; temperature; energy budget

INTRODUCTION

Feeding is a tool for energy transport throughout the biosphere. Thus, measurement of feeding rates and energy intake is a basic task in quantitative ecology and physiology. Because of operational expense, experimental determinations of exact feeding rates throughout the development of decapod crustacean larvae are scarce. Daily consumptions of newly hatched Artemia nauplii have been chiefly estimated by manual counting during one single day of instar periods (Yatsuzuka, 1962; Inoue, 1965; Levine & Sulkin, 1979; Cronin & Forward, 1980; Johns, 1982; Emmerson, 1984; Yufera et al., 1984). A few investigators have given some information about the state of development of experimental crab larvae (Johns & Pechenik, 1980; Dawirs, 1983; Paul & Nunes, ’ Contribution to research project An-145/1-l granted by Deutsche Forschungsgemeinschaft 0022-0981/86/$03.50 0 1986 Elsevier Science Publishers B.V. (Biomedical Division)

(DFG).

134

RALPH R. DAWIRS AND ANDREAS DIETRICH

1983). To our knowledge, only Kurata (1960), Mootz & Epifanio (1974), Wienberg (1982), and Anger & Dietrich (1984) have measured daily feeding rates during successive moulting cycles of decapod crustacean larvae. A preliminary energy budget has been presented for all larval stages of Carcinus maenas (Dawirs, 1983). Feeding rates were determined once per instar, and cumulative food intake was estimated by multiplying with mean stage duration times. Energy values for the prey, newly hatched Artemia nauplii, were taken from the literature. It seems very unlikely, however, that feeding rates do not change within one moulting cycle. Variations in larval energy intake may greatly influence growth, respiration, excretion, and consequently energy budget efficiences. Therefore, daily dynamics of larval feeding rates have to be recorded, in order to understand partitioning and utilization of energy and biomass during larval development. In the present study Carcinw mae~ L. larvae were fed newly hatched Artemia nauplii. Feeding rates were measured on a daily basis from hatching through metamorphosis at different temperatures. Temperature-dependent “mean nutritive values” of single newly hatched Artemia nauplii were determined, relative to a 24-h feeding regime.

MATERIAL

OBTAINING AND HANDLING

AND METHODS

OF LARVAE

Ovigerous ~r~~~ maenas females were collected from the rocky intertidal region of northern Helgoland in July 1983 and taken to the laboratory. Maintenance of gravid crabs, and larval collecting and handling methods, follow standardized procedures described by Dawirs (1982). Individual larvae were kept in small glass vials containing 20 ml of filtered (1 pm) natural sea water from Heigoland (31 to 33x0 S), in constant 12,15,18 or 25 “C. They were fed newly hatched brine shrimp nauplii, Artemia spp. (San Francisco Bay Brand, Inc., Newark, California). Sets of 50 individually reared larvae were used to measure temperature-dependent larval development (stage durations). A reasonable amount of larvae were reared at each temperature as stock culture for food consumption experiments. FEEDING RATES

Food consumption was measured at 12, 15, 18, and 25 “C on a daily basis from hatching through metamorphosis of Carcinw maenas. By using a pipette 100 newly hatched Artemia nauplii were put into each of 10 replicate glass vials containing 10 ml sea water. Crab larvae were allowed to feed for 24 h until they were transferred to experimental vials prepared the same way. The remaining Artemia nauplii were killed by adding concentrated formaldehyde. Dead nauplii were collected from the bottom of

LARVAL

FEEDING

RATES

OF CARCINUS

MAENAS

135

the vials and pipetted into 1.5 ml micro test tubes (Eppendorf, 3810), where they were finally stored in 4% formaldehyde. The Artemia nauplii, remaining after 24-h feeding, were counted by automatic image analysis using a Quantimet 23C with a Plumbicon scanner (Cambridge Scientific Instruments Ltd.) in interface with a Digital PdP 1l/23 computer (Digital Equipment Corporation) and a Zeiss Tessovar photomicroscope. The method and background theory has been published by Dietrich & Uhlig (1984). Image analysis measures the total projected area of a sample. Mean area per nauplius is determined by scanning 50 intact nauplii out of a sample. This was done once for every 10 replicates to minimize errors due to variations between different hatches. By knowing the mean area per nauplius and biomass data, one derives the number of individuals and total biomass in a sample. Results are given as numbers of nauplii, biomass and energy consumed. Carcinus maenas larvae do not always eat 100% of every Artemia nauplius caught. Thus, fragments of varying numbers and size are detected, which cannot be quantified by manual counting. Therefore automatic image analysis proved to be more reliable and effective. To assess losses of nauplii by methodical implications, the above described experimental procedure was repeated 100 times with no crab larvae feeding. As a result 96.75 f 0.53 nauplii were recorded. Thus, the feeding rate (FR) was over-estimated by 3.25 nauplii per sample. Any further results were corrected by this factor. BIOMASS

OF ARTEMIA

NAUPLII

Biomass (dry weight, DW; elemental carbon, C; nitrogen, N; hydrogen, H) of newly hatched (0 h) and l-day-old (24 h) Artemia nauplii was measured at 6, 9, 12, 15, 18, or 25 ‘C. Ten replicates with 200 nauplii per analysis were carried out respectively, a total of 24000 nauplii were measured in 120 analytical samples. Glass tibre filters (RCTWhatman, GF/C, 0.8 cm diameter) were ashed in an annealing furnace at 500 “C for 5 h. After cooling they were weighed on a UM 3 (Mettler) to the nearest 0.11.18 and stored in a desiccator. The nauplii were pipetted into a clean dish containing filtered sea water and poured on a glass Bbre filter connected with a low vacuum. Adherent salts were removed by rinsing with water from the ion exchanger. Samples (filter and nauplii) were put into pre-ashed and pre-weighed Ag-cartridges, deep frozen and then dried at < lop2 mbar in a GT2 (Leybold-Heraeus) for a minimum of 3 h. After drying, the cartridges were immediately closed and put into a desiccator over silica gel, where they were stored until analysis. Dry weight was determined by a UM 3 (Mettler) to the nearest 0.1 pg. Elemental analyses (C, N, H) were carried out with an Elemental Analyser Model 1106 (Carlo Erba Science) using cyclohexane-2.4-dinitrophenylhydrazone as standard. Energy equivalents were calculated by the N-corrected formula given by Salonen et al. (1976) and expressed in Joules (1 J = 0.239 cal.).

TABLE I

DW (w)

DW ols) C olg) N Ug) H olg) C (%) N (%) H (%) C:N J.ind.-’ J.mg DW-’

C Gue) N (II@;) H 018) C (%) N (%) H (%) C:N J . ind. - ‘ J.mg DW-’

+ 0.055 + 0.017 + 0.004 + 0.012 + 0.85 + 0.20 + 0.41 -f: 0.08

2.883 1.407 0.253 0.215 48.80 8.78 7.48 5.56 0.057 19.63

+ 0.019 rt: 0.010 + 0.004 + 0.004 + 0.30 & 0.12 + 0.11 F 0.05

Oh

2.843 1.360 0.258 0.234 47.82 9.09 8.26 5.27 0.054 19.04

Oh

15°C

6°C

+ 0.046 t 0.014 + 0.003 i_ 0.004 + 0.73 + 0.17 + 0.16 t 0.07

2.723 1.300 0.246 0.208 47.56 9.03 7.66 5.21 0.05 1 18.88

i 0.079 k 0.028 + 0.004 ) 0.008 + 1.03 + 0.22 + 0.41 +_0.05

24 h

2.796 1.354 0.258 0.242 48.43 9.23 8.65 5.25 0.054 19.40

24 h i f i f f f + +

2.882 1.406 0.255 0.248 48.61 8.80 8.57 5.52 0.056 19.52

0.048 0.029 0.006 0.018 0.81 0.30 0.55 0.14

f 0.060 k 0.022 rt: 0.005 f 0.007 f 0.69 f 0.20 ) 0.21 f 0.07

Oh

2.867 1.403 0.261 0.226 48.94 9.11 7.87 5.38 0.057 19.71

Oh

18°C

9°C

+ 2 f + + f + k

2.720 1.293 0.250 0.220 48.02 9.27 8.19 5.18 0.052 19.16

0.035 0.013 0.003 0.003 0.47 0.13 0.13 0.05

f 0.068 f 0.014 + 0.003 f 0.005 of:0.56 f 0.12 + 0.16 f 0.03

24 h

2.800 1.388 0.263 0.211 49.65 9.38 7.54 5.28 0.056 20.15

24 h

2.944 1.420 0.264 0.227 48.25 8.96 7.71 5.39 0.057 19.30

?; 0.064 + 0.017 2 0.004 & 0.012 & 0.88 + 0.19 & 0.39 + 0.04

-.

+ 0.038 + 0.014 & 0.004 t_ 0.003 & 0.56 i: 0.11 + 0.08 F 0.04

Oh

2.824 1.444 0.274 0.222 51.10 9.70 7.84 5.27 0.059 21.05

Oh

25°C

12 “C

---

& 0.048 + 0.013 t 0.002 f: 0.008 rt 0.83 rt 0.16 f 0.29 & OTO7

2.559 1.187 0.259 0.187 46.44 10.11 7.32 4.59 0.047 18.22

+ 0.040 * 0.014 i: 0.004 r 0.003 i: 0.54 f 0.11 t_ 0.08 & 0.03

24 h

2.818 1.359 0.254 0.203 48.04 9.00 7.22 5.31 0.054 19.17

24 h

dry weight (DW), carbon (C), nitrogen (N), and hydrogen (H) content of newly hatched (0 h) and one-day-old Artem& nauplii (24 h) at 6, 9, 12, 15, 18, 25 “C; energy values (individual and DW-related) in Joules; percentages related to individual DW; mean r 95% confidence interval.

Arremia spp.: individual

LARVAL FEEDING RATES OF CARCINUS MAENAS

137

STATISTKCS

Mean values were computed as arithmetic means + 95% confidence interval and time-dependent trends described by means of least square regressions, with correlation coefficients tested for significant differences from zero. Mean b&es were compared by t-test with preceding F-test (Sachs, 1974).

RESULTS BIOMASS OF FOOD ORGANISMS (ARTEMIA NAUPLII)

The instar I nauplii ofArtemia spp. are not yet able to consume any food (Sorgeloos, 1980). Consequently they were losing biomass. Table I presents results of elemental and DW analysis of newly hatched and 24 h old nauplii at 6, 9, 12, 15, 18, 25 “C. Temperature-dependent losses reveal signiticant trends in DW and C content:

DKm, (a) = -0.117 + 0.018 T(“C) (r= 0.888, P
c A24h(pg)

= - 0.075 + 0.012 T (“C) (r = 0.978, P < 0.001)

The six determinations for newly hatched nauplii result in mean initial values of 2.874 + 0.043 pg DW and 1.407 + 0.028 fig C. By this, “mean nutritive values” of Artemiu nauplii were estimated, calculating temperature-dependent DW and C losses during the fast 24 h (Table II). Since no significant trends were found for N and H losses, these data were pooled. Mean nutritive values calculated were, 0.258 + 0.004 rug N and 0.220 + 0.011 pg H, irrespective of temperat~e. Because energy contents were calculated from DW and C data (Salonen et al., 1976), they also slightly decrease with increasing temperature. Results did not indicate any signitlcant losses at 6 “C. Table II summarizes temperature-dependent mean specific nutritive values of individual newly hatched Artemia nauplii during a 24-h feeding regime. TABLE II

Artemia spp.: temperature-dependent “mean nutritive value” of newly hatched Artemia nauphi, due to a 24-h feeding regime of Car&us muenus larvae; individual dry weight (DW), carbon (C), nitrogen (N), and hydrogen (H) content of Artemii nauplii 12 h after hatching; energy vahres (~~~du~ and DW-related) in Joules; temperature ( ” C).

DW Olg) C olg) N tig) J-J olg) J - ind. - * J.mg DW-’

6°C

9°C

12°C

15°C

18 “C

25 “C

2.874 1.407 0.258 0.220 0.057 19.73

2.853 1.391 0.258 0.220 0.056 19.61

2.827 1.373 0.258 0.220 0.055 19.50

2.801 1.355 0.258 0.220 0.054 19.39

2.775 1.338 0.258 0.220 0.054 19.27

2.115 1.296 0.258 0.220 0.052 19.00

138 FEEDING

RALPH R. DAWIRS AND ANDREAS DIETRICH RATES OF CARCINUS

MAENAS

LARVAE

Original data on FR are presented in Figs. l-4. Variances of individual daily feeding rates proved to be high through all larval stages at any temperature, with a dramatic

Age (days)

Fig. 1. Curcinus muenus: individual daily larval feeding rates, in numbers of newly hatched Aftemia nauplii consumed; original data as mean f 95% confidence interval, at 12 “C.

Megalopa

LO 36 32 28

Zoea-C

2

L

6

Age (days) Fig. 2. As Fig. 1: at 15°C.

LARVAL FEEDING

RATES OF CARCINUS MAENAS

139

68 64 60 56 52 LB LL LO 36 32

B e

28

2

21

x 0 2

20 16 12 8

if! 3 2: o 3

4 0

Zoea-L

28 2L 20 16 12 8 I.

2

c

2

L

6

610

0

Age (days) Fig. 3. As Fig. 1: at 18°C.

increase when megalops were fed at 25 “C. Larval FR follow a general trend, but somewhat less distinct in earlier stages at lower temperatures. During moulting cycles C. maenus larvae achieve highest FR within the first 2 days at any temperature. After this, larvae continue feeding but at steadily decreasing rates, approaching zero shortly before ecdysis. The daily amount of food consumed shortly after ecdysis increases with increasing temperature. This trend ends between 18 and 25 “C. On the following days larvae reduce daily food consumption more rapidly at bigher temperatures, due to accelerated development. The largest amount of food ingested by a single C. maena.s larva was measured for a megalopa in a replicate at 18 ’ C, 74 Artemia nauplii on Day 2.

140

RALPH R. DAWIRS AND ANDREAS DIETRICH Megalopa

Zoea-4

I

72

1 68

:6L :60

136

s z

:32

\-

28

i

3 5

12.L 20

\;

116 :I2 -8 c

Age (days) Fig. 4. As Fig. 1: at 25 “C.

Energy and biomass ingested by each larval instar are listed with reference to experimental temperature in Table III. Despite occasional significant over- or undershooting (22, Z3), food consumption per instar increases exponentially with time (Fig. 5B, Table IV). The accumulated amount of food, however, which single larvae have ingested on successive days since hatching, is best described by power functions (Fig. 5A, Table IV). In both cases temperature-dependent stage durations are considered (Table V). At higher temperatures less food is consumed during complete zoea development, resulting in 7~63% less energy intake at 25 “C than at 12 “C (P < 0.001). Unlike zoeae, megalops, however, consume more food during moulting cycles at higher temperatures. This is true between 12-18 “C (P < O.OOl), but is reversed between 18-25 “C. Megalops feed on about as much Artemiu nauplii at 25 and 15 “C, but with

LARVAL FEEDING RATES OF CARCI~~~ MAENAS

141

TABLE III

Cur&us maenus: total amount of food ingested during single larval instars, zoea-I (Zl) to megalops (M), zoea (X2”), and total larvai development (X”) at 12,1.5,18, and 25 “C: numbers ofArremia nauplii (n), dry weight (DW), carbon (C), nitrogen(N), hydrogen (H), and energy (Joule) ingested; mean f 95 y0 confdence interval. 12°C

18°C

15°C

25°C

Zl

D”W C N H Joule

47.21 f 133.46 f 64.82 + 12.18 + 10.39 f 2.60 f

7.87 22.25 10.80 2.03 1.73 0.44

21.40 + 3.35 59.93 + 9.38 28.99 + 4.54 5.52 -f. 0.87 4.71 f 0.74 1.16 & 0.18

15.40 + 42.73 + 20.60 k 3.97 * 3.39 + 0.82 +

22

D”vv C N H Joule

60.23 f 170.28 + 82.70 + 15.54 f 13.25 + 3.12 1

7.08 20.01 9.72 1.82 1.56 0.39

23.63 + 6.93 66.18 2 19.42 32.02 + 9.39 6.10 + 1.79 5.20 + 1.52 1.28 at: 0.38

23.56 f 4.73 65.38 + 13.i3 31.52 f 6.33 6.08 f 1.22 5.18 & 1.04 1.26 i 0.25

23

Dz, C N H Joule

47.75 f 5.47 134.98 + 15.44 65.56 f 7.50 12.32 i 1.41 10.51 & i.20 2.63 f 0.30

80.25 k 224.79 i: 108.74 + 20.71 + 17.66 + 4.36 i

12.35 34.59 16.73 3.18 2.72 0.67

60.20 + 167.06 f 80.55 f 15.53 + 13.25 f 3.22 f

9.33 25.88 12.48 2.40 2.05 0.50

12.03 f. 6.26 32.66 + 16.99 15.59 f 8.11 3.10 of: 1.62 2.65 & 1.38 0.62 + 0.32

24

DnW C N H Joule

90.42 + 255.61 f 124.14 f 23.33 + 19.89 + 4.98 +

10.00 28.26 13.73 2.58 2.20 0.55

63.80 + 178.71 + 86.45 + 16.46 + 14.04 f 3.47 +

8.83 24.74 11.97 2.28 1.95 0.48

65.72 f t82.38 f 87.94 f 16.96 + 14.46 + 3.52 +

12.23 33.93 16.36 3.16 2.69 0.66

38.55 + 11.20 104.67 & 30.39 49.96 + 14.51 9.95 & 2.89 8.48 f 2.46 1.99 + 0.58

M

D”W C N H Joule

169.58 k 479.40 f 232.83 + 43.75 k 37.31 f 9.34 +

20.72 58.58 28.45 5.34 4.56 1.15

209.01 + 36.97 585.43 + 103.56 283.20 + 50.09 9.54 53.92 f 45.98 + 8.13 11.35 + 2.01

228.97 f 635.38 + 306.36 k 59.07 + 50.37 * 12.25 f

41.38 114.84 55.37 10.68 9.11 2.22

209.16 + 567.87 + 270.45 + 53.96 + 46.02 + 10.79 *

64.79 175.89 83.77 16.72 14.26 3.34

cz4

D”W C N H Joule

244.64 f 691.59 f 335.89 f 63.12 f 53.82 + 13.48 f

17.78 50.28 24.42 4.59 3.91 0.98

189.09 f 529.64 + 256.22 f. 48.79 + 41.60 + 10.27 f

164.87 + 457.51 + 220.59 F 42.54 + 36.27 + 8.82 *

IS.09 50.20 24.21 4.67 3.98 0.97

91.27 + 264.08 + 126.06 F 25.10 + 21.40 f 5.02 f

24.24 65.82 31.42 6.26 5.33 1.25

CM

D”W C N H Joule

310.99 + 844.33 + 403.04 f 80.24 + 68.42 + 16.05 f

99.60 270.43 129.09 25.70 21.91 5.14

415.20 f 37.59 1173.78 + 106.25 570.07 f 51.60 107.12 + 9.70 91.34 + 8.27 22.88 k 2.07

25.74 72.08 34.87 6.64 5.66 1.40

397.24 + 57.95 1112.66 of:162.31 538.26 + 78.52 102.49 * 14.95 87.39 * 12.75 21.57 + 3.15

5.05 14.01 6.75 1.30 1.11 0.27

389.55 f 76.69 1081.00 & 212.81 521.22 t 102.61 100.50 + 19.79 85.70 f 16.87 20.84 k 4.10

18.26 + 49.57 + 23.66 + 4.71 + 4.02 + 0.94 +

2.75 7.47 3.57 0.71 0.6I 0.14

30.38 & 7.46 82.48 & 20.24 39.28 + 9.64 7.84 + 1.92 6.68 + 1.64 1.57 + 0.39

142

RALPH R. DAWIRS AND ANDREAS DIETRICH

less biomass and energy intake at 25 “C!. Nevertheless, total food consumption from hatcbingtbrough metamorphosis is significantly lower at bigher temperatures, witbin the present temperature range. About 23 J are consumed during the whole larval life at

1

Cumulative

2

Consumption-pq.instar

daily consumption

B

400

g

350

;

300 250 200

$ 3 fl 5

150

? iz

100

2.

50

3

12

15

16

12

25 Temperature

15

18

g 6 E -

25

I’C)

Fig. 5. Car&us maenus: time and temperature-dependent cumulative food consumption during larval development; A, cumulative numbers of Artemia nauplii consumed on successive days of larval development; B, total numbers ofArtemiu nauplii consumed during successive larval instars; solid lines are regressions given in Table IV.

TABLE IV Curcinus maenas: time-dependent (t, days) larval food consumption (C) at different temperatures (“C); cumulative numbers ofAtiemia nauplii consumed on successive days of larval development are described by power functions (A); total numbers of Ariemia nauplii consumed during successive larval instars are described by exponential functions (B); a and b = constants; r = correlation coefficient; P = level of significance; *P < 0.05; ** P < 0.01; *** P < 0.001; ****P < 0.0001; NS, not significant; for further explanation see Fig. 5.

lnC=a+b.lnr

12 15 18 25

In C = a + br (B)

(A) --

Temp. (“C)

a

0.972 - 0.228 -0.816 - 0.083

1.216 1.663 1.978 1.769

b

0.999 0.992 0.997 0.983

**** *** *** **

3.471 2.620 2.157 f.843

0.025 0.065 0.108 0.131

0.933 0.941 0.982 0.842

* * ** NS

LARVAL FEEDING RATES OF CARCZNUS MAENAS

143

12 ‘C (z 63 days), and only w 16 J at 25 ‘C (a 32.5 days) (P < 0.01). Thus, cumulative larval energy input decreases by x 30% while development rate accelerates by almost 63%.

TABLE V

Carcinus maenas: stage duration times of successive larval instars (zoea-1 to megalops) and cumulative development (days) (cum.) at 12, 15, 18, and 25 “C; mean + 95% confidence interval (CI); n, numbers of larvae moulting to the next stage shown in parentheses. 12°C Zoea-I Zoea-2 cum. Zoea-3 cum. Zoea-4 cum. Megalopa cum.

10.70 + 0.67 9.92 + 0.49 20.50 k 1.00 9.00 f 0.58 29.50 i: 1.19 13.00 f 0.56 41.58 + 1.32 23.89 + 2.09 63.11 ?r 2.89

15 “C (37) (36) (36) (25) (9)

6.87 i 0.34 6.21 f 0.33 13.07 + 0.56 5.98 -fr0.25 19.10 + 0.59 7.55 + 0.47 26.66 + 0.80 15.73 + 1.09 42.15 f 1.44

18°C (46) (43) (40) (38) (26)

5.87 k 5.00 f 10.47 + 4.45 f 14.86 + 5.30 * 20.22 + 10.15 + 30.45 f

0.50 0.39 0.65 0.28 0.88 0.40 1.11 0.63 1.59

25°C (36) (30) (29) (23) (20)

5.14 + 0.37 3.94 + 0.50 9.00 4 0.59 2.94 + 0.27 11.94 it: 0.69 3.77 f 0.43 15.77 + 1.00 7.50 4 1.96 23.50 + 3.17

(22) (18) (18) (17) (6)

At 12 “C megalopa development takes % 38% of total larval development time (Table V). During this period megalops contribute 41% to the accumulated larval energy input from hatching through metamorphosis (Table III, Fig. 5). Megalops can be considered as the major energy consumers in larval development. This percentage contribution dramatically increases at higher temperatures. At 25 ’ C, 67 % of the whole energy requirement for larval development is consumed by megalops, while the pro~~on~ stage duration only takes = 32 %. In other words, megalops may require about twice as much energy to support development, than all four zoeal stages together.

DISCUSSION

The brine shrimp eggs obtained from San Francisco Bay Brand, Inc. Newark, California, were said to originate from San Francisco Bay. We measured mean DW for newly hatched Artemiu nauplii, 2.87 + 0.04 ,ug. This is within the range of values, analysed for more than 17 Artemia strains from 14 countries (Vanhaecke & Sorgeloos, 1980, 1983). Nevertheless, our data differ significantly from DW of nauplii originating from San Francisco Bay eggs, 1.63 + 0.11 pg (SFB l), 1.61 k 0.09 pg (SFB 2) (Vanhaecke & Sorgeloos, 1980), 1.85 pg (Benjits et al., 1976), 1.66 rt 0.07 pg (Anger & Dietrich, 1984); Oppenheimer & Moreira (1980) determined 2.76 pg (DW) for first instar Artemia nauplii (San Francisco Bay), comparable with our fmdings. The brine shrimp nauplii we applied in feeding experiments, show best correspondence to newly hatched Artemiu spp. originating from Great Salt Lake, 2.70 + 0.13 pg (GSL 1)

144

RALPH R. DAWIRS

AND ANDREAS

DIETRICH

(Vanhaecke & Sorgeloos, 1980). Since the company in Newark also delivers eggs from the Salt Lake Brine Shrimp, Inc. Grantsville, Utah (Cat. No. 36495), perhaps we received Salt Lake brine shrimp eggs packed in the wrong can. Artemia nauplii lose DW with 2 to 13% (6 to 25 “C) during 24 h after hatching. Comparable values have been reported in the literature, 4 to 20% in 12 to 20 “C (Paffenhofer, 1967; Benjits et al., 1976; Anger & Dietrich, 1984). During the course of our experiments, individual brine shrimp nauplii lose energy by rates up to 17.5% (25 ‘C). Absolute biomass and energy losses of food organisms were low compared with relatively high individual variation in daily larval feeding rates of Carcinus maenas. Nevertheless, we calculated temperature-dependent “mean nutritive values” of newly hatched Artemia nauplii, for higher accuracy of energy intake data. The fairly large individual variation we observed in C. rnaenas larval FR seems to be a general phenomenon in Anomura (Kurata, 1960) and Brachyura (Anger & Dietrich, 1984). Crab larvae, however, reveal species-specific features in individual FR. Menippe mercenaria show increasing FR on successive days of zoeal instars, with higher rates in later stages. Daily food intake reaches maximum values at the start of megalopa development and decreases towards metamorphosis (Mootz & Epifanio, 1974). Paralithodes camtschatica zoea-1 to zoea-3 reveal comparable trends, with slightly decreasing FR at the end of each moulting cycle. Decreasing daily food intake on successive days of zoea-4 might be an artefact, due to experimental implications, since there was no survival of a megalopa (Kurata, 1960). Changes in FR during moulting cycles of Hyas araneus larvae are conspicuously different (Anger & Dietrich, 1984). Daily food intake by zoeae follow smoothly shaped parabolae with time, slightly increasing during postmoult and inter-mot&, and decreasing towards ecdysis during premoult. FR lack similar clear figures in megalops. Nevertheless, all three larval stages of H. araneus lower the daily amount of food ingested during moulting cycles (Anger & Dietrich, 1984). Patterns of Carcinus maenas larval FR are strikingly different from each of the discussed species. Maximum rates are achieved within 1 or 2 days after moulting, approaching almost zero towards ecdysis. Comparing Menippe mercenaria, Hyas araneus and Carcinus maenas, there appears to be no general way to describe FR through moulting cycles of brachyuran crab larvae. It will be up to future surveys, to examine if at least similar patterns can be determined on the family or genus level. Absolute numbers ofArtemia nauplii consumed by larvae of Paralithodes camtschatica (Kurata, 1960), Menippe mercenaria (Mootz & Epifanio, 1974) Hyas araneus (Anger & Dietrich, 1984), and Carcinus maenas (present study) are comparable and within one order of magnitude. Total food intake is less in C. maenas larvae (Table III), than in Men&e mercenaria (z 1335 nauphi at 25 “C) and Hyas araneus larvae (Z 1100 nauplii at 12 “C) (Mootz & Epifanio, 1974; Anger & Dawns, 1982). As a common feature in all three species, megalops appear to be the major energy consumers in larval life. In proportion to total larval development, megalops consume z 54% (Menippe mercenaria at 25 c C), 49% (Hyas araneus at 12 ‘C), and 4 1y0 (Carcinus maenas at 12 ’ C) of all Artemia nauplii ingested. C. maenas megalops even achieve proportions of 67% at

145

LARVAL FEEDING RATES OF CARCZNUS ~AENAS

25 “C. This is not, however, true for decapod larvae in general, as shown by .#%gurus bernhardus megalops, which do not feed during the entire moulting cycle (Dawirs, 198 1, 1984). Although initial FR of Curcinus muenas larval stages increase with temperature, less total amount of food is consumed due to accelerating development (Tables III, V). The

AFR lZoeo -1

AZoea-3

,2

oZoe0 -2

AZoea -4

*‘c’

e Megolopa

is Temperature PC1 Fig. 6. Carcinus menus: temperature-dependent average daily feeding rates (AFR) related to single stages, zoea-1 (Zl) to megalops (M), zoea (P), and total larval development (Z”); AFR = mean numbers of Artemiu nauplii (n) consumed per day at different temperatures (‘C); regressions are given in Table VI. TABLE VI Car&us maenas: temperature-dependent (T, “C) average daily feeding rates (AFR) of single stages, zoea-I (Z-l) to megalops (M), zoea (X2’) and total larval development (Z”); a,, a,, and a, = constants; for further r = correlation coeflkient; P = level of si~i~c~ee; * P < 0.05; ** P K 0.01; NS, not si~~c~t; explanation see Fig. 6.

AFR = a, + a,T + a,T2

-QO

z-1 z-2 z-3 z-4 M Z&4 P

15.103 21.783 - 60.259 - 20.262 - 48.753 - 8.931 - 20.239

Ql - 1.292 - 2.043 8.215 3.155 6.011 1.801 3.025

f

P

0.033 0.059

0.997 0.955

- 0.226 - 0.077 -0.118 - 0.048 - 0.067

0.983 0.919 0.991 0.986 0.991

** * * NS ** * **

02

146

RALPH R. DAWIRS AND ANDREAS DIETRICH

same is true in temperature-dependent larval FR of Purulithodes camtschatica (Kurata, 1960) and Pandulus borealis (Wienberg, 1982). Fig. 6 and Table VI present average feeding rates (AFR) of single larval stages (Z I-M), cumulative zoeal development (~““) and total larval development (CM). Temperature-dependent AFR describes larval ability to counterbalance increasing metabolic costs for maintenance at higher water temperatures (Dawirs, 1983). As yet we cannot explain variable AFR-figures in zoeae. Megalops reveal almost steadily increasing AFR with temperature, indicating that even high temperatures (“tide pool conditions”) are not limiting development. AFR-CM approaches maximum values between 18-25 “C, and AFR-xZ4 even decreases at temperatures > 18 ‘C. Curcinus maenus zoeae thus show limited ability to compensate for higher maintenance costs by suflicient feeding, when water temperatures exceed x 18 “C. Because C. maenus zoeae will rarely meet temperatures > 18 ‘C in Helgoland waters, while megalops may advance into occasionally “heated” intertidal shallow waters, AFR proves to be a response adapted to habitat requirements (Dawirs, 1985). Calculations of AFR from data in Kurata (1960) and Wienberg (1982) lead to comparable temperature-dependent responses in larvae of Paralithodes camtschatica and Pandalus borealis. The characteristic changes in FR during Curcinus muenus larval moulting cycles (Figs. l-4) show that measuring consumption only once per instar results in highly misleading estimations of total consumption. Previous estimations (Dawirs, 1983) over-rated the total amount of energy consumed by the five larval stages by x 36%. Improved energy-based total budget efliciences (18 “C) are 3 1% in assimilation, and 4.4% in gross growth (K,), which still seems to be comparably low (see references in: Dawirs, 1983; Anger & Dietrich, 1984). Investigations on temperature-dependent changes in respiration, excretion, and growth rates, during the course of C. maenus larval moulting cycles, have been finished recently (in prep.). This information shall further improve and differentiate our understanding of crab larval energetics.

ACKNOWLEDGEMENTS

We would like to thank Dr. E. Wahl and Mr. M. Janke for providing Artemiu nauplii and Ms. F. Schom for technical assistance. Elemental analyses were carried out by Ms. C. Piischel. Ms. B. Seeger provided secretarial assistance. Our thanks are due to Dr. M. Rieper for correcting the English manuscript. REFERENCES ANGER, K.

& R.R. DAWIRS, 1982.Elemental composition (C, N, H) and energy in growing and starving larvae of Hyus uruneus (Decapoda : Majidae). Fish. Bull. NOAA, Vol. 80, pp. 419-433. ANGER, K. $ A. DIETRICH, 1984. Feeding rates and growth efficiencies in Hyus araneus L. larvae (Decapoda : Majidae) reared in the laboratory. J. Exp. Mar. Bid. Ecol., Vol. 77, pp. 169-181.

LARVAL FEEDING

RATES OF CARCINUS MAENAS

147

BENJITS,F., E. VANVCK)RDEN & P. SORGELOOS,1976. Changes in the biochemical composition ofthe early larval stage of the brine shrimp, Artemia salina L. In, 10th European Symposium on Marine Biology, Vol. 1,

edited by G. Persoone 8r E. Jaspers, Universa Press, Wetteren, Belgium, pp. l-9. CRONIN,T. W. & R. B. FORWARD,JR., 1980. The effects of starvation on phototaxis and swimming of larvae of the crab Rhithropanopeus harrkvii.Biol. Bull. (Woo& Hole. Mass.), Vol. 158, pp. 283-294. DAWIRS,R. R., 1981. Elemental composition (C, N, H) and energy in development of Pagurus bernhardus (Decapoda : Paguridae) megalopa. Mar. Biol., Vol. 64, pp. 117-123. DAWIRS, R.R., 1982. Methodical aspects of rearing decapod larvae, Pagurus bemhardus (Paguridae) and Carcinus maenas (Portunidae). Helgol. Meeresunters., Vol. 35, pp. 439-464. DAWIRS, R.R., 1983. Respiration, energy balance and development during growth and starvation of Carcinus maenas L. larvae (Decapoda : Porttidae). J. Exp. Mar. Biol. Ecol., Vol. 69, pp. 105-128. DAWIRS, R.R., 1984. Respiratory metabolism of Pagurus bemhardus (Decapoda : Paguridae) megalopa. Mar. Biol., Vol. 83, pp. 219-233. DAWIRS, R.R., 1985. Temperature and larval development of Carcinus maenas (Decapoda) in the laboratory; predictions of larval dynamics in the sea. Mar. Ecol. Prog. Ser., Vol. 24, pp. 297-302. DIETRICH,A. & G. UHLIG, 1984. Stage specific classification of copepods with automatic image analysis. Crustaceana, Suppl. Vol. 7, pp. 159-165. EMMERSON,W. D., 1984. Predation and energetics ofPenaeur indicus (Decapoda : Penaeidae) larvae feeding on Brachionus plicatilis and Artemia nauplii. Aquaculture, Vol. 38, pp. 201-209. INOUE, M., 1965. On the relation of amount of food taken to the density and size of food and water temperature in rearing the phyllosoma ofthe Japanese spiny lobster, Panulimsjaponicus (V. Siebold). Bull. Jpn. Sot. Sci. Fish., Vol. 31, pp. 902-906. JOHNS, D. M., 1982. Physiological studies on Cancer irroratus larvae. III. Effects of temperature and salinity on the partitioning of energy resources during development. Mar. Ecol. Prog. Ser., Vol. 8, pp. 75-85. JOHNS, D.M. & J.A. PECHENIK, 1980. Influence of water-accommodated fraction of No. 2 fuel oil on energetics of Cancer irroratus larvae. Mar. Biol., Vol. 55, pp. 247-254. KURATA,H., 1960. Studies on the larva and post-larva of Paralithodes camtschatica. II. Feeding habits of the zoea. Bull. Hokkaido Reg. Fish. Res. Lab., Vol. 21, pp. 1-8. LEVINE,D. M. & S. D. SULKIN, 1979. Partitioning and utilization of energy during larval development of the xanthid crab Rhithropanopeus harrisii (Gould). J. Exp. Mar. Biol. Ecol., Vol. 40, pp. 247-257. MOOTZ,C. A. & C. E. EPIFANIO,1974. An energy budget for Menippe mercenaria larvae fed Artemia nauplii. Biol. Bull. (Woods Hole, Mass.), Vol. 146, pp. 44-45. OPPENHEIMER,C. H. & G. S. MOREIRA,1980. Carbon nitrogen and phosphorus content in the development stages of the brine shrimp Artemia. In, The brine shrimp Artemia, Vol. 3, edited by G. Persoone et al., Universa Press, Wetteren, Belgium, pp. 365-373. PAFFENH~FER, G.-A., 1967. Caloric content of larvae of the brine shrimp Artemia salina. Helgol. Wiss. Meeresunters., Vol. 16, pp. 130-135. PAUL, A.J. & P. NUNES, 1983. Temperature modification of respiratory metabolism and caloric intake of Pandalus borealis (Kroyer) first zoeae. J. Exp. Mar. Biol. Ecol., Vol. 66, pp. 163-168. SACHS, L., 1974. Angewandte Statistik. Springer, Berlin, pp. 554. SALONEN,K., J. SARVALA,I. HAKALA& M.-L. VILJANEN,1976. The relation of energy and organic carbon in aquatic invertebrates. Limnol. Oceanogr., Vol. 21, pp. 724-730. SORGELOOS,P., 1980. The use of the brine shrimp Artemia in aquaculture. In, The brine shrimp Artemia, Vol. 3, edited by G. Persoone et al., Universa Press, Wetteren, Belgium, pp. 25-46. VANHAECKE,P. & P. SORGELOOS,1980. International study on Artemia. IV. The biometrics of Artemia strains from different geographical origin. In, The brine shrimp Artemia, Vol. 3, edited by G. Persoone et al., Universa Press, Wetteren, Belgium, pp. 393-405. VANHAECKE,P. & P. SORGELOOS,1983. International study on Artemia. XXX. Bio-economic evaluation of nutritional value for carp (Cyprinus carpio L.). Larvae of nine Artemia strains. Aquaculture, Vol. 32, pp. 285-293. WIENBERG,R., 1982. Studies on the influence of temperature, salinity, light and feeding rate on laboratory reared larvae ofdeep sea shrimp, Pandalus borealis (Kroyer, 1838).Meeresforschung., Vol. 29, pp. 136-153. YATSUZUKA,K., 1962. Studies on the artificial rearing of the larval brachyura, especially of the larval blue-crab, Neptunus pelagicus Linnaeus. Rep. Vsa Mar. Biol. Stat., Vol. 9, pp. l-88. YUFERA,M., A. RODRIGUEZ& L.M. LUBIAN, 1984.Zooplankton ingestion and feeding behavior 0fPenaeu.s kerathurus larvae reared in the laboratory. Aquaculture, Vol. 42, pp. 217-224.