Growth and Development of Calanus Finmarchicus

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Growth and development of Calanus finmarchicus related to the influence of temperature: Experimental results and conceptual model Francois Carlotti, Michael Krause, Günther Radach

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Francois Carlotti, Michael Krause, Günther Radach. Growth and development of Calanus finmarchicus related to the influence of temperature: Experimental results and conceptual model. Limnology and Oceanography Bulletin, American Society of Limnology and Oceanography, 1993, 38 (6), pp.1125- 1134. 10.4319/lo.1993.38.6.1125. hal-02987456

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Growth and development of Calanusfznmarchicus related to the influence of temperature: Experimental results and conceptual model Fraqois Carlotti Observatoire des Sciences de l’univcrs, Station Zoologique URA CNRS 7 16, UniversitC Paris VI/INSU/CNRS, B.P. 28, 06230 Villefranche-sur-Mer, France, and Institut fur Meercskunde, Universitlt Hamburg, Troplowitzstr. 7, 2000 Hamburg 54, Germany

Michael Krause Institut fur Allgemeine Botanik, UniversitHt Hamburg, Ohnhorststr. 18, 2000 Hamburg 52

Giinther Radach Institut fur Meereskundc, Universitat Hamburg

Abstract A large number of weight values for the different stages of Calanus finmarchicus permits us to show that no overlapping takes place between ranges of structural weights (i.e. without storage) of successive copcpoditc stages at a given temperature and that structural growth is exponential at all temperatures. Nevertheless, in each instar, weights are negatively correlated with temperature. The hypothesis of critical molting weights is discussed in the framework of the elaboration of a conceptual model coupling growth and development.

To estimate the production of copepods, and deviations of the mean growth curve and mean more generally zooplanktonic production, we development time. There are other sources of must know the common characteristics of variability of weights of copepods. Numerous growth and development for the individuals observations of copepods in situ have revealed of the same population and the sources of their strong seasonal variability of weight for adults variability. Weight integrates the whole feed- and late instars (Comita et al. 1966; Tande ing history and the influences of physical pa- 1982; Grigg et al. 1989), supposedly due to rameters on physiology. The development as temperature or food supply, or both. In this a whole appears as a succession of identical paper, we analyze the influence of temperature phases for all individuals of the same popu- on the observed weights of Calanus jinmar- lation. For crustaceans, development in each chicus for each stage. stage includes a phase of tissue differentiation In a model coupling growth and develop- followed by a growth phase (Skinner 1985), ment of small copepods, Carlotti and Sciandra and the passage into a new stage depends on (1989) suggested that molting, within a given one or more signals (e.g. metabolisms, hor- stage, takes place at a fixed weight, called the monal productions). “critical molting weight.” In other words, un- In all studies of population dynamics, the der given temperature and food conditions, the individuals of a population exhibit variability individuals present a range of weights between in growth and time of development, even in the critical weights on entering and leaving this stable conditions (Bamstedt 1988). This phe- stage. Carlotti and Sciandra supposed that these notypic variability is expressed by standard critical weights could be changed by temperature and food supply, and proofs for this critical molting weight were given for small co- Acknowledgments We thank Detlef Quadfascl for letting us work with the pepods by a literature review in which the range temperature profiles corresponding to M.K.‘s samplings. of weights for a given instar did not overlap Paul Nival, Beat Gasser, Suzanne Nival, and John Dolan that of the previous and the next instar. Here are acknowledged for reviews and comments on the manu- we test whether the above assumption is also script. This work was supported by the French-German co- acceptable for large copepods. As an example, operation program PROCOPE in the form of a grant for we take C. finmarchicus because it plays an a stay to F.C. at the Institut fur Mccrcskunde (Hamburg). important ecological role in the marine envi- 1125 1126 Carlotti et al. ronment, being the preferred prey of cod and van Arkel 1980; Williams and Lindley 1980). haddock, and dominates the zooplankton in Temperature was at 6°C in the homogeneous large parts of the oceans (Williams and Lindley water column at the beginning of cohort de- 1980; Smith 1988). It is extensively studied, velopment, whereas mixed-layer temperatures and numerous weight data of the stages are of 8-9°C had developed when the copepods available to derive common rules of growth were maturing into stage CV and adults. and development. Results of Harris ( 198 3) and The third group corresponds to values from McLaren (1986) support the hypothesis of a the Norwegian coast (Tande 1982, figure 5; critical molting weight for this species but only Bamstedt and Ervik 1984; Bamstedt 1988) and for the structural weight, thus without storage. Fram Strait (Smith 1988, 1990), concerning McLaren (1986) showed that no overlap takes essentially CV, males, and females. place between the ranges of structural weights McLaren et al. (1989) and Smith (1988, of successive copepodite stages at 5°C and that 1990) used a chemical preservation method, structural growth of C. Jinmarchicus is expo- but corrected the dry weight estimates for an nential at this temperature. average loss of 25 and 26%, respectively. Oth- To test the critical molting weight hypoth- ers stored their samples by deep-freezing or esis and McLaren’s exponential-growth hy- weighed animals freshly sampled. pothesis in a large range of temperatures, we Original data -Krause’s data originated used weights of C. jnmarchicus from two from three different stations in the North Sea sources. The first is a nonexhaustivc review of between 1982 and 1985 and from grouped published weights of C. jinmarchicus, the sec- stations in the Fram Strait region between East ond source is data collected by M. Krause dur- Greenland and Svalbard in 1984. Parts of the ing several cruises. data from the North Sea (1983-l 984) and data from Fram Strait have been published (Katt- Materials and methods ner and Krause 1987; Kattner et al. 1989). Review of literature- To compare the weight Those papers reported the lipid and wax ester values found in the literature, we distinguish contents as well as the fatty acid and alcohol three regional groups. The first group is mainly composition of C. jinmarchicus and Calanus constituted of results from the NW Atlantic hyperboreus. Stations, sampling methods, by McLaren (1986) and McLaren et al. (1989) counting, storing and drying methods, and lip- with the temperature values of McLaren and id analysis have also been described in detail Corkett (1986, figure 3). McLaren (1986, figure (Kattner andKrause 1987; Kattner et al. 1989). 1) presented ranges of body weights discount- The unpublished data used here have been ing the variable lipid storage, which is taken obtained following the same methods and cov- in reference in our study. For summer, we con- ering a longer period, from 1982 to 198 5. The sidered the temperature above the thermocline data were related to temperature according to (see figure 2 of McLaren et al. 1989). We add the following procedure. At all stations, we weight values used by Davis (1987) for mod- have profiles of temperature. At most stations, eling. we obtained vertical distributions of the dif- The second group consists of values ob- ferent stages from bottle samplers. Since there tained in the North Sea. We collected values is no direct information about the amplitude obtained from in situ sampling either in var- of the diel vertical migration, it was extrapo- ious seasons (Gauld 195 1; Marshall and Orr lated from investigations of Krause and Ra- 1956; Hirche 1983; Grigg et al. 1989) or ob- dach (1989). Thus, when the vertical distri- tained for 1 yr (Marshall and Orr 19 5 5; Comita bution of a stage was known, we took the et al. 1966). Corner et al. (1967) presented val- temperature corresponding to the depth of ues for body nitrogen of individuals cultivated maximum abundance. When no clear peaks at 10°C from egg to adult. Values given in C appeared (case of CV), we took the mean tem- and N were converted to dry weight considered perature of the water where we found individ- respectively as 50 and 10% of dry weight. From uals. When vertical distributions were un- the Fladen Ground experiment FLEX’76, dry known, either the water column was weights of C. finmarchicus were estimated by isothermal, and we used this temperature val- different investigators (Daro 1980; Franz and ue, or the water column presented a thermo- - Calanus growtl tl vs. temperature 1127

Cline. In this latter case, the hypothesis was A’ Marshall’ ’ & On’ 1956’ made, following Williams and Lindley (1980) cl Comer et al. 1967 and Krause and Radach (1989), that CI-CIV Fransz & van Arkel 1980 I I 3.5) : Davis 1987 were above the thermocline (thus we used the Hirche 1990 I I I t mean temperature in the mixed layer), and CV, adult males, and females were distributed over the entire water column, in which case we used a mean value of temperature of the whole water column. Results Literature data -The literature review in- dicates that weights of naupliar stages are sel- dom studied. Figure 1 presents values from egg to NVI. Egg weights range from 0.25 to 0.6 pg. Runge’s value (cited by McLaren et al. 1989) appears higher than the others. Only two complete sets for the entire naupliar development were found (Fransz and van Arkel 1980; Davis 1987). Corner et al. (1967) investigated groups, Egg N I N II N III N IV N V N VI C I namely eggs, NI-NII, NIB-NIV, NV-NVI, but the numbers of determinations are very dif- Developmental instars ferent for these groups (one measure for NIII- Fig. 1. Growth of Calanus finmarchicus from egg to NIV, 14 for NI-NII). Their values appear close NW. Growth curves of Calanuspaczjicus (Fernandez 1979), to those of Davis. Nevertheless, his values Calanus sinicus (Uye 1988) and CaIanus helgolandicus must be considered cautiously because they (Mullin and Brooks 1970) added for comparison. were derived from length data connected to weight by a power curve. Because their weigh- ing was performed with great numbers of in- stage coincide with the lower limits of the next dividuals, particularly for the first four stages, instar over the whole range of temperatures. the weight values of Fransz and van Arkel The weights in all stages have slightly negative (1980) give a complete and reliable set (see correlations with temperature. Weight ranges their tables 1 and 4). Their set clearly shows a of CV, adult males, and females are compa- decrease of weight after hatching. rable. Some values of CV at 15°C seem higher Values in the literature for CI-CIII (Fig. 2) than others, but, as described in the methods, fall into the weight range presented by Mc- it is possible to attribute this to individuals Laren ( 1986). For CIV (Fig. 2) and for CV, below the thermocline, where temperatures of adult females, and adult males (Fig. 3), liter- -6OC are found. Two groups of stage CV are ature values exceed the upper limit of the range clearly separated by the thermocline. of structural weight measured by McLaren Synthesis of the data-All data have been (1986), but rarely the lower one. Variability in grouped in a semilogarithmic graph of weight CV weight seems very important, particularly vs. relative time (Fig. 5). Relative time has for populations living in cold waters. Thus, been defined by Corkett et al. (1986) assuming following McLaren (1986) weights of CI-CIII equiproportional development. Because equi- are only structural, whereas we must consider proportional development means that the du- a storage compartment for CIV, CV, and adults. ration of a given stage occupies a constant pro- It is possible to discern an influence of tem- portion of the embryonic development time perature only for the values of females. across temperature, we can introduce weight Original data-Krause’s data (Fig. 4) are in vs. temperature graphs for each instar in the good agreement with the preceding values. graph with weight vs. relative time. We have They showed that for a given temperature there kept the ranges of structural weights presented is no overlap between weights of instars from by McLaren (1986) and plotted two straight CI to CV. Moreover, upper limits of a given lines against the limits of these ranges. Figure 1128 Carlotti et al.

CI 10 CI lo- . A Marshd%h 1956 0 McLaren 1986 Groupe!dvalues l McLaren et al. 1989 q Comeret al. 1967 n Davis 1987 8- A Dare 1980 8 . A Fransz & van Arkel 1980 6- 0 Williams & Lindley 1980 1 Cl 4 A El 2 tA 1 01 OA 0 9 18 0 9 18 0 9 18 14 CII CII 14- CII 1 12 - .

lo- R : 8-

0 9 18 -0 9 18 30: c III 30 c III 301 c III 1, . n Gauld 1951 25 : s

6 20: . . . .IIii 0 . . ‘. i 15: 0 GI2 25:;I R 10 10 A 1 5- 5 L 0 9 18 0 9 18 0 9 18 c IV 120 1201 0 c IV 120 . c IV 100 100 l Tande 1982 1 0 1 . 80 cl . 60 .I R 6o :..

40 .Y l I . 20 20L l 0 9 18 0 9 18 0 18 Temperature (“C) Temperature (“C) Temperkre (“C) Fig. 2. Dry weights of stages CI-CIV of Calanus finmarchicus vs. temperature based on literature data. Straight lines correspond to the ranges of structural weights found by M&u-en (1986, figure 1). Calanus growth vs. temperature 1129

cv Grouped values l Willi~s~ Lmdlev 1980 ’ 0 Comitattl. 1966 a Smith 1988 A Fransz & van Arkel 1980 - l Grigg et al. 1989 . Smith 1990 + o Comer et al. 1967 . A Marshall &C~T 1955 0 BAmstedt LErvik 1984 A Daro 1980 0 BAmstedt 1988 m Gauld 1951 A Tande 1982 + Hirche 1983 ’ A

0- 0 9 18

6001 Ad. females 1 Ad. females 1 Ad. females 1 Ad. males Adults

0 9 18 0 18 0 18 0 Temperature (“C) Temperahe (“C) Temperahe (“C) T!mperakre (& Temperakre (&

Fig. 3. As Fig. 2, but of stages CV, adult females, and adult males of Calanusfinmarchicus.

5 shows that growth of C. finmarchicus is ex- Naupliar growth curves for other species of ponential, at least for its structural part. The Calanus largely agree with values for C. jin- heaviest CIII, CIV, and CV exceed the upper marchicus. Among the three other species pre- limits of structural weight in the proportions sented, Calanus helgolandicus is certainly the of 23, 120, and 200%, respectively. These pro- species closest to C. jinmarchicus (Bradford portions could be attributed to increased stor- 1988). age in these stages, which would correspond Growth of copepodites-The comparison be- to 19, 54, and 66% of their dry weight. tween the data and the range of structural weight obtained by McLaren (1986) suggests Discussion that the whole weight is essentially structural Growth of nauplii- As stated by McLaren et for the first three copepodite stages, and stor- al. (1989), knowledge about growth of the nau- age represents a large part of weight in CIV pliar stages is insufficient. It will be difficult to and CV and in adults. Heavier CVs exceed the appreciate the ecological role of nauplii with- upper limit of structural weight found by out better knowledge of their growth and de- McLaren (1986) by 200%. In other words, velopment. Judging from the literature re- stores should correspond to 66% of dry weight. viewed, it is likely that the values of Fransz This value is in very good agreement with re- and van Arkel(l980) for the stages from eggs sults of Hakanson (1984, figure 1) on the lipid to NV (their NV1 value seems suspiciously low) contents of copepodite stages of Calanus pa- and the values of Marshall and Or-r (1956) for cz~cus. Figure 2 also clearly shows that the NIV-NV1 yield the most realistic growth curve highest variability in CV weights occurs in the of the naupliar phase of C. finmarchicus (Fig. data obtained from Fram Strait and the Nor- 1). The curve confirms that the weight decreas- wegian coast- the coldest waters. Part of this es from eggs to NII due to the inability of these variability of weights in CV is due to over- stages to feed (Marshall and Orr 1955) and wintering observed for the population at very shows the important growth rate during stage high latitudes. The animals stay in deep water NIII to recover the loss of weight during the in winter and metamorphose into adults in previous nonfeeding stages, as shown for Cal- spring (Bamstedt and Tande 1988). Tande anus marshallae (Peterson 1986). ( 1982) showed a decrease in dry weight (300- 1130 Carlotti et al.

120: 120: CI c II 120 120 cIII . c IV Gi 1oo : DW = 10.78 - 0.89 T loo : DW = 10.48 - 0.54 T 1oo DW = 29.69 - 1.19 T 1 100: s E 80: 80: b A 80 80:’ P f 60: 60: 1 B 601 60- 1 1 40: 40: I 401 A 40 : : 20: 20 y A Ol~~l...l.~ 0 Yr2=s0 20 :

0: 0 4 8 12 16 0 4 8 12 16 0- 0 4 8 12 16 0 4 8 12 16

600 Ad. females 600 Ad. males DW = 88.95 - 3.45 T DW = 286.13 - 14.25 T DW = 304.77 - 14.84 T DW = 261.63 - 8.89 T 500 500

100

0-- Ol------0 4 8 12 16 0 4 8 12 16 0 4 8 12 16 0 4 8 12 16 Temperature (“C) Temperature (“C) Temperature (OC) Temperature (“C) Fig. 4. Dry weights of the copepodites and adults of Calanus finmarchicus vs. temperature from three stations in the North Sea (A, Cl, m and from Fram Strait (0). For each stage, the equation of the least-square regression is given.

108 pg) in CV from December to March, cou- molting from one instar to the following instar pled to a change in chemical composition and occurs at a fixed critical structural weight, which the onset of sexual differentiation in stage CV. depends on temperature. The values also show Thus, we can suppose utilization of stores in- that the correlation of temperature with body ducing a decrease of N 64% of dry weight. Such weight is negative. Such a correlation has been a value falls into the range of lipid content of shown by Corkett and McLaren ( 1978, figure C. hyperboreus (Conover 1962). The fat re- 27) for Pseudocalanus. Moreover, they showed serves of stage CV go directly into egg for- that the percentage of reduction in length per mation by adult females (Bamstedt and Tande “C increased with stage. If we graph the slopes 1988), and the grazing of females permits con- of the regressions of dry weight vs. temperature tinuity of spawning (Kattner et al. 1989). (W = a - bT) obtained in Fig. 4 for consec- Krause’s values (Fig. 4) show no overlap be- utive stages, we also obtain such an increase tween the weight ranges of consecutive instars with stage (Fig. 6A). It is more convenient to from CI to CV at a given temperature. These normalize each regression coefficient with the values are adequate to validate the hypothesis origin of the regression (Fig. 6B). The variance of critical molting weights because for both the of slope (6) and origin of regression (a) could North Sea and Fram Strait the lipid content be calculated from residual variance in the re- of individuals was low in all stages, as can be gression and from these estimates the variance seen in table 2 of Kattner and Krause (1987) of b : a (relative slope) has been calculated. The and in table 2 of Kattner et al. (1989). Thus, standard deviation is indicated in Fig. 6B. A Calanus growth vs. temperature 1131

Ad. males Ad. females

0 4 8 12 16 Temperature

0 4 8 12 16 04 81216 0 4 8 12 16 Temperature Temperature Temperature

1 1.25 1.53 1.81 2.11 2.72 Relative time Fin. 5. Synthesis of the data of Figs. 2, 3, and 4 in a semilogarithmic graph: weights vs. relative time as defined by Corkett et ai. (1986).

Bartlett test (Sokal and Rohlf 198 1) has shown exponential growth for C. paczjkus, and results that variances of b : a for the different copepod of Vidal(l980) do not present overlap between stages are not significantly heterogeneous (P = ranges of copepodite weights. It is probably 0.05). The relative slopes of CIII, CIV, and more difficult to prove exponential growth adult males are not significantly different (P = phases for species with multiyear cycles, be- 0.05), but they are different from CV and adult cause growth stops for long periods. Never- females which are themselves not significantly theless, weight ranges of Calanus glacialis different. It is suggested that the relative slope shown by Slagstad and Tande (1990, figure 4) for CI is different from others; however, the do not exhibit overlap, and growth seems ex- data are too few to take the statistical result as ponential from CI to CIV in the period from a strong hypothesis. For the same reason the spring to summer. Similar relations may be value of the relative slope for CII cannot be hidden by the high variability in the data of considered. Bottrell and Robins (1984) for C. helgolandi- McLaren (1986) suspected that adequate cus. Nevertheless McLaren (1986), using their tests of the exponential-growth hypothesis data, found agreement with the exponential- barely exist, but the grouped data of Fig. 5 growth hypothesis. allow such a test. A short literature review con- A good way to test these hypotheses exper- cerning growth of other Calanus species con- imentally would be the use of Calanus species firms the hypotheses of exponential growth and that have little lipid storage. For instance, Cal- of critical molting weights. For C. marshallae, anus sinicus (Uye 1988) has exponential Peterson (1986, figure 7) showed exponential growth, and ranges of weights do not overlap growth and no overlap between ranges of stage between successive stages. Moreover, mean weights from NIV to CIII, but overlap between body lengths in each stage are negatively cor- CIIT-CIV and CIV-CV. Frost (1980) suggested related with temperature. 1132 Carlotti et al.

max total wt

max stfuctuml wt

initial wt entering age

U i I I I I I I I I C I C II C III C IV C V Female Male Fig. 7. Suggested time scales of structural and storage components during the molt cycle in an instar for different Stages temperature conditions.

the growth rate between structural weights Wi and Wi-11. These critical weights are lower for high temperatures than for low temperatures, and the observed weights in a stage appear to be negatively correlated with temperature. The observed total body weight is the sum of the structural weight and the lipid content. From the physiological point of view, it is sufficient to consider the structural weight in the molting process because hormones of molting (ecdy- sone) act on young tissues with cells having a high potential of multiplication (Skinner 1985). Afterward, these cells will have a phase of dif- I I I I I I I I C I C II C III C IV C V Female Male ferentiation and will grow during the molting cycle. Stages McLaren (1986, p. 1345) said that “it is un- likely that weight variations in nature can be Fig. 6. A. Comparison of the effect of temperature on understood without identification of cohorts, dry weight of copepodites and adult stages, using the slope of the regressions (b) from Fig. 4. Vertical lines-standard recognition of resting stages, and separation of deviation. B. Effect of temperature on the weight-specific the lipid ‘store’ from other components.” To ratio (b : a). Vertical lines-standard deviation. Horizontal test the model suggested from this analysis, it lines join means that are not significantly different (see would be interesting to repeat his experimental text). work for different temperatures, distinguishing between structural weight and lipid stores, to Conceptual model of growth within each see if the time scales of development of these stage-To summarize the results of our data compartments during the course of the indi- analysis, we suggest the following conceptual vidual molt cycle are consistent with our con- model (Fig. 7). A copepod enters in stage with i ceptual model. a structural weight Wi. Then the structural body weight grows (exponentially if the external References conditions are good) until a maximum structural weight is reached, which is the critical BAMSTEDT, U. 1988. Ecological significance of individual variability in copepod bioenergetics. Hydrobiologia structural weight for the next stage Wj+, . Thus, 167/168: 43-59. development is linked to structural growth, and -, AND A. ERVIK. 1984. Local variation in size and the time of development in stage i depends on activity among Calanus jinmarchicus and Metridia Calanus growth vs. temperature 1133

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way: Generation cycles, and variation in body weight WILLIAMS, R., AND J. A. LINDLEY. 1980. Plankton of the and body content of carbon and nitrogen related to Fladen Ground during FLEX ‘76. 3. Vertical distri- overwintering and reproduction in the copepod Cal- bution, population dynamics and production of Cal- anusjnmarchicus (Gunner-us). J. Exp. Mar. Biol. Ecol. anusfinmarchicus (Crustacea, Copepoda). Mar. Biol. 62: 129-142. 60: 47-56. UYE, S. 1988. Temperature-dependent development and growth of Calanus sinicus (Copepoda: Calanoida) in the laboratory. Hydrobiologia 167/168: 285-293. VIDAL, J. 1980. Physioecology of zooplankton. 1. Effects of phytoplankton concentration, temperature and body Submitted: 13 May 1991 size on the growth rate of Calanus pacificus and Pseu- Accepted: 23 September 1992 docalanus. Mar. Biol. 56: 111-134. Revised: 8 December 1992