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Development rate of copepod eggs of the genus Calanus
J. exp. mar. Biol. EC&., 1972, Vol. 10, pp. 171-175; @ North-Holland Publishing Company
DEVELOPMENT RATE OF COPEPOD EGGS OF THE GENUS CALANUS C.
J. CORKETT
Marine Biological Association of zke United Kingdam, Tke Laborafory, Citadel Hi& P~ymoatk, England Abstract. The development time to hatching of eggs of four closely related species of copepods, Calanrrs keigafandicus (Claus), C. jimnarckicas (Gunn.), C. glacialis Jaschnov, and C. kyperboreus Kr6yer as a function of temperature is given by t> = a(T-a)*. The constant a is positively correlated with egg diameter, so that large eggs take longer to develop than small eggs. The vatue of the constant a is related to the geographical range of the species.
INTRODUCTION
The development time (0) in days from laying to hatching of copepod eggs is well represented as a function of temperature T (in “C) by Bzlehrhdek’s (1935) equation D = a(T-a)*, where a, CIand b are constants (~cLaren, 1966; McLaren, Corkett & Zillioux, 1969). It has been known for some time that among closely related organisms Iarge eggs tend to develop more slowly than small eggs. Dannevig (1895) reported that, for five species of fish eggs he investigated, larger eggs required a longer incubation time than smaller eggs and BerriIl(l935) showed this to be true for a large number of ascidian species: the same seems to be true among closely reIated forms of copepods since, excluding a population from Ogac Lake, there is a significant correlation between the value of a and egg diameter in Pseudocaianus minutus (McLaren, 1966). This correlation does not apply to distantly related species, e.g., eggs of the genus Calanus, although much larger than those of Pseudocalanus minutus, develop much more rapidly (McLaren, 1966). The present work consists of an ex~rime~tal study of the rate of development of the eggs of Calanus he~golandicus (Claus); the data are considered relative to that for three other species of this genus. METHOD
The experimental methods used here for the hatching of eggs have been given in detail by Corkett (1970). Each experiment involved a group of eggs produced within a 2-h period by female C. helgolandicus collected off Plymouth on 24th May 1971. The eggs were placed in vials and kept in water baths, the temperatures of which were taken every 2 h. All eggs were observed every 2 h and the time of hatching of 50 % of the group of eggs was determined. The salinity of the sea water, taken from outside the breakwater across the mouth 171
C‘. J. CORKETT
I72
of Plymouth
Sound,
was not determined,
but the influence
of salinity
on development
rate is probably negligible within natural ranges (McLaren, Walker & Corkett, 1968). It was observed that all the eggs laid by one particular female of C. hefgofundicus possessed membranes similar to those reported for some individuals of C. finmarchicus from Tromso by Marshall & Orr (1953) and for some eggs of C’. hyperboreus (Conover, 1967). Although such eggs of C. hefgokmdicus were identical in size (excluding the membrane) with other eggs of C. helgolundicus they were not used in any of the experiments. RESULTS
The results on the rate of development of C. helgolandicus eggs are summarized in Table I which clearly shows that the development time increases with decreasing temperature. Initially five replicates were set up at each temperature but only those in which more than 50 ‘A of the eggs hatched have been included in Table 1. As is -,-AHLE
Development Number of experiments
i
time to hatching of eggs of Calanus
Number of eggs
Mean experimental temperature with standard error
( ‘0 2 3 3 4
IO 24 24 43
0.7*0.032 3.9 .+0.007 7.4 +0.072 14.2 tO.O1O
ltelyo/undiicus.
Time for 50 “; hatching of viable eggs (days) Mean
Kange
5.91 4.20 7.41 1.37
6.5 ~7.31 3.87-4.87 2.0 .2.66 I .08-l .74
clear from the table there was a greater mortality at the lower temperatures and at 0.7 “C only 10 eggs hatched in two experiments. One experiment at 3.9 “C, not included in the table, gave a mean development time of 7.42 days. The same female which laid eggs for this experiment at 3.9 “C, laid eggs that were also used for experiments at 7.4 “C, and these eggs hatched within the range of value given in Table I; it was decided that this one value of 7.42 days should be considered abnormal and excluded from calculations. Table I shows the mean values of development time in days: the original data consisting of the individual values for C. helgolandicus were used for the fitting of BtlehrBdek’s equation. After conversion to logarithms the regression of D on T was calculated giving for the eggs of C. helgolundicus log b = 2.407 -- 1.71 log (T+ 7.52) or b = 255(T+ 7.52)- I.” (Fig. 1A). Similar regressions were calculated for C. glaciufis and C. hyperboreus using the data of McLaren, Corkett & Zillioux (1969) and for C. jkmarchicus from Scotland and Norway by combining the mean development times at each temperature given by Marshall & Orr (1953); the regression equations
DEVELOPMENT
173
RATE OF COPEPOD EGGS
r
100 -
IO-
z
0” -
3
D
-
I-
Fig. 1. B8ehradek’s function fitted to development times of eggs of Calanus helgolundicus: ordinates give development time in days and abscissae temperature in “C minus the biological zero (a): A, after conversion to logarithms the regression of D on T was calculated without a mean b giving log B = 2.407-1.707 log (T+7.52) or b = 255(T+7.52)- 1 ‘I; B, a regression similarly calculated but with a mean b giving log b = 1.872-1.355 log (T+4.92) or b = 74.5(T+4.9)-1.35: l values of individual experiments the means of which are given in Table I; o experiment that was considered abnormal (see p. 172).
are given in column A in Table II. The value of b was then assigned a constant mean value formed from the mean of the previous values for b (column A, Table II) and the equations refitted by the least squares method (Fig. 1B). When b is given a mean value then the value of a (which describes differences in slope and is the intercept on the ordinate of a log temperature-log development time plot) is correlated with egg size. The actual value given to b although altering the equations does not affect the TABLE II
BHehradek’s function fitted to development Species Calanus jinmarchicus C. helgolandicus C. glacialis C. hyperboreus
A Equation without mean b D D D D
= = = =
27.7(T+4.57)-‘.‘O 255(T+7.52)-1.71 28.8(T+5.0)-0.94 374(T+11.1)-‘.67
time of eggs of four species of copepods.
B Equation with mean b D D D D
= = = =
67.4(T+6.71)-‘.= 74.5(T+4.92)-I.= 113(T+8.45)-‘.35 121(T+8.51)-1.35
Reference
Marshall & Orr (1953) Present work McLaren et al. (1969) McLaren et al. (1969)
C. J. CORKETT
174
main argument. Other values of b have been chosen for marine - 1.68 was used by McLaren (1966) and - 2.05 by McLaren,
calanoid copepods; Corkett & Zillioux
(1969) Corkett & McLaren (1970) and Corkett (1970). Table 11 shows that the value of a (column B) increases with egg diameter (Table III). The regression of ~1on egg diameter (x) is B = - 129.8+ 1.32 x (I) where x is the egg diameter
in /t. The correlation
coefficient
is 0.95.
Size of eggs of the genus Cu/mus Species
Size with standard error (,u)
Reference
Culanus jinmurchicus
145 163.9 :L 0.866 178.63 2.5 190 ’
Marshall & Orr ( 1953) Present worli McLaren (1966) McLaren et rrl. (I 969)
C. helgolandicus C. glacialis C. hyperboreus
’ Only one egg was measured.
DISCUSSION
The larger eggs of C. hyperboreus and C. glacialis take longer to develop than the smaller eggs of C.jinmarchicus and C. helgolandicus, i.e. the value of a in Belehradek’s equation is positively related to egg diameter (equation 1). Since a and b are known for an egg of given size (equation 1 and Table II), one can determine a by measuring the development time D at one temperature T and using Belehradek’s equation. This will be sufficient to predict the development time D for any other temperature T. A possible explanation for the linear relationship between development time corrected for differences in a (equation 1) is that development rate is determined by the surface : volume ratio which decreases with increasing diameter. One could think that the metabolic exchange between the egg and its external environment is relatively slower for the larger eggs with their relatively smaller sraface. Alternatively, one might assume that the development rate is determined by metabolic processes related to the size of the internal surfaces which in turn is proportional to the external surface. The value of a (which is often called the biological zero and is the theoretical temperature at which development is infinitely long) seems to be related to the geographical range of the species and presumably, therefore, to water temperature. Distributions of the species are given by Matthews (1969), Colebrook (1964) and Colebrook, GIover & Robinson (1961). Under the classification given by Colebrook, Glover & Robinson (1961) the distribution would be as follows: C. glacialis and C. hyperboreus - northern oceanic (a z - 8.5 “C), C. jinmarchicus - northern intermediate (CI = - 6.7 “C), C. helgolandicus - southern intermediate (a = - 4.9 “C).
DEVELOPMENT RATE OF COPEPOD EGGS
175
ACKNOWLEDGEMENTS
I should like to thank Dr R. P. Harris for his assistance during this work and Drs H. Meves and I. A. McLaren for reading the manuscript and making helpful suggestions. Mr D. K. Grif5ths and Mrs Helen Egginton assisted with the operation of the computer programmes. This work was carried out while the author was on a Fellowship from N.E.R.C. REFERENCES
BELEHRADEK, J., 1935. Temperature and living matter. Protoplasma Monographia, No. 8, Borntraeger, Berlin, 277 pp. BERRILL,N. J., 1935. Studies in tunicate development. Part III. Differential retardation and acceleration. Phil. Trans. R. Sot. Ser. B, Vol. 225, pp. 255-326. COLEBROOK,J. M., 1964. Continuous plankton records: a principal component analysis of the geographical distribution of zooplankton. Bull. mar. Ecol., Vol. 6, pp. 78-100. COLEBROOK, J. M., R. S. GLOVER& G. A. ROBINSON,1961. Continuous plankton atlas of the northeastern Atlantic and the North Sea. Bull. mar. Ecol., Vol. 5, pp. 67-80. CONOVER,R. I., 1967. Reproductive cycle, early development and fecundity in laboratory populations of the copepod Calanus hyperboreus. Crustaceana, Vol. 13, pp. 61-72. CORKETT,C. J., 1970. Techniques for breeding and rearing marine calanoid copepods. Helgoliinder wiss. Meeresunters., Bd 20, S. 318-324. CORKETT,C. J. & I. A. MCLAREN, 1970. Relationships between development rate of eggs and older stages of copepods. J. mar. biol. Ass. U.K., Vol. 50, pp. 161-168. DANNEVIG,H., 1895. The influence of temperature on the development of the eggs of fishes. Rep. Fishery Bd Scotl., 1894, Part 3, pp. 147-152. MARSHALL,S. M. & A. P. ORR, 1953. Calanusfinmarchicus: egg production and egg development in Tromse Sound in spring. Acta Boreal., A. Sci., Vol. 5, pp. 1-21. MATTHEWS,J. B. L., 1969. Continuous plankton records: the geographical and seasonal distribution of Calanusfinmarchicus s. 1. in the North Atlantic. Bull. mar. Ecol., Vol. 6, pp. 251-273. MCLAREN, I. A., 1966. Predicting development rate of copepod eggs. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 131, pp. 457-469. MCLAREN, I. A., D. A. WALKER& C. J. CORKETT,1968. Eflects of salinity on mortality and development rate of eggs of the copepod Pseudocalanus minutus. Can. J. Zool., Vol. 46, pp. 1267-1269. MCLAREN, 1. A., C. J. CORKETT& E. J. ZILLIOUX, 1969. Temperature adaptations of copepod eggs from the Arctic to the Tropics. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 137, pp. 486493.
DEVELOPMENT RATE OF COPEPOD EGGS OF THE GENUS CALANUS C.
J. CORKETT
Marine Biological Association of zke United Kingdam, Tke Laborafory, Citadel Hi& P~ymoatk, England Abstract. The development time to hatching of eggs of four closely related species of copepods, Calanrrs keigafandicus (Claus), C. jimnarckicas (Gunn.), C. glacialis Jaschnov, and C. kyperboreus Kr6yer as a function of temperature is given by t> = a(T-a)*. The constant a is positively correlated with egg diameter, so that large eggs take longer to develop than small eggs. The vatue of the constant a is related to the geographical range of the species.
INTRODUCTION
The development time (0) in days from laying to hatching of copepod eggs is well represented as a function of temperature T (in “C) by Bzlehrhdek’s (1935) equation D = a(T-a)*, where a, CIand b are constants (~cLaren, 1966; McLaren, Corkett & Zillioux, 1969). It has been known for some time that among closely related organisms Iarge eggs tend to develop more slowly than small eggs. Dannevig (1895) reported that, for five species of fish eggs he investigated, larger eggs required a longer incubation time than smaller eggs and BerriIl(l935) showed this to be true for a large number of ascidian species: the same seems to be true among closely reIated forms of copepods since, excluding a population from Ogac Lake, there is a significant correlation between the value of a and egg diameter in Pseudocaianus minutus (McLaren, 1966). This correlation does not apply to distantly related species, e.g., eggs of the genus Calanus, although much larger than those of Pseudocalanus minutus, develop much more rapidly (McLaren, 1966). The present work consists of an ex~rime~tal study of the rate of development of the eggs of Calanus he~golandicus (Claus); the data are considered relative to that for three other species of this genus. METHOD
The experimental methods used here for the hatching of eggs have been given in detail by Corkett (1970). Each experiment involved a group of eggs produced within a 2-h period by female C. helgolandicus collected off Plymouth on 24th May 1971. The eggs were placed in vials and kept in water baths, the temperatures of which were taken every 2 h. All eggs were observed every 2 h and the time of hatching of 50 % of the group of eggs was determined. The salinity of the sea water, taken from outside the breakwater across the mouth 171
C‘. J. CORKETT
I72
of Plymouth
Sound,
was not determined,
but the influence
of salinity
on development
rate is probably negligible within natural ranges (McLaren, Walker & Corkett, 1968). It was observed that all the eggs laid by one particular female of C. hefgofundicus possessed membranes similar to those reported for some individuals of C. finmarchicus from Tromso by Marshall & Orr (1953) and for some eggs of C’. hyperboreus (Conover, 1967). Although such eggs of C. hefgokmdicus were identical in size (excluding the membrane) with other eggs of C. helgolundicus they were not used in any of the experiments. RESULTS
The results on the rate of development of C. helgolandicus eggs are summarized in Table I which clearly shows that the development time increases with decreasing temperature. Initially five replicates were set up at each temperature but only those in which more than 50 ‘A of the eggs hatched have been included in Table 1. As is -,-AHLE
Development Number of experiments
i
time to hatching of eggs of Calanus
Number of eggs
Mean experimental temperature with standard error
( ‘0 2 3 3 4
IO 24 24 43
0.7*0.032 3.9 .+0.007 7.4 +0.072 14.2 tO.O1O
ltelyo/undiicus.
Time for 50 “; hatching of viable eggs (days) Mean
Kange
5.91 4.20 7.41 1.37
6.5 ~7.31 3.87-4.87 2.0 .2.66 I .08-l .74
clear from the table there was a greater mortality at the lower temperatures and at 0.7 “C only 10 eggs hatched in two experiments. One experiment at 3.9 “C, not included in the table, gave a mean development time of 7.42 days. The same female which laid eggs for this experiment at 3.9 “C, laid eggs that were also used for experiments at 7.4 “C, and these eggs hatched within the range of value given in Table I; it was decided that this one value of 7.42 days should be considered abnormal and excluded from calculations. Table I shows the mean values of development time in days: the original data consisting of the individual values for C. helgolandicus were used for the fitting of BtlehrBdek’s equation. After conversion to logarithms the regression of D on T was calculated giving for the eggs of C. helgolundicus log b = 2.407 -- 1.71 log (T+ 7.52) or b = 255(T+ 7.52)- I.” (Fig. 1A). Similar regressions were calculated for C. glaciufis and C. hyperboreus using the data of McLaren, Corkett & Zillioux (1969) and for C. jkmarchicus from Scotland and Norway by combining the mean development times at each temperature given by Marshall & Orr (1953); the regression equations
DEVELOPMENT
173
RATE OF COPEPOD EGGS
r
100 -
IO-
z
0” -
3
D
-
I-
Fig. 1. B8ehradek’s function fitted to development times of eggs of Calanus helgolundicus: ordinates give development time in days and abscissae temperature in “C minus the biological zero (a): A, after conversion to logarithms the regression of D on T was calculated without a mean b giving log B = 2.407-1.707 log (T+7.52) or b = 255(T+7.52)- 1 ‘I; B, a regression similarly calculated but with a mean b giving log b = 1.872-1.355 log (T+4.92) or b = 74.5(T+4.9)-1.35: l values of individual experiments the means of which are given in Table I; o experiment that was considered abnormal (see p. 172).
are given in column A in Table II. The value of b was then assigned a constant mean value formed from the mean of the previous values for b (column A, Table II) and the equations refitted by the least squares method (Fig. 1B). When b is given a mean value then the value of a (which describes differences in slope and is the intercept on the ordinate of a log temperature-log development time plot) is correlated with egg size. The actual value given to b although altering the equations does not affect the TABLE II
BHehradek’s function fitted to development Species Calanus jinmarchicus C. helgolandicus C. glacialis C. hyperboreus
A Equation without mean b D D D D
= = = =
27.7(T+4.57)-‘.‘O 255(T+7.52)-1.71 28.8(T+5.0)-0.94 374(T+11.1)-‘.67
time of eggs of four species of copepods.
B Equation with mean b D D D D
= = = =
67.4(T+6.71)-‘.= 74.5(T+4.92)-I.= 113(T+8.45)-‘.35 121(T+8.51)-1.35
Reference
Marshall & Orr (1953) Present work McLaren et al. (1969) McLaren et al. (1969)
C. J. CORKETT
174
main argument. Other values of b have been chosen for marine - 1.68 was used by McLaren (1966) and - 2.05 by McLaren,
calanoid copepods; Corkett & Zillioux
(1969) Corkett & McLaren (1970) and Corkett (1970). Table 11 shows that the value of a (column B) increases with egg diameter (Table III). The regression of ~1on egg diameter (x) is B = - 129.8+ 1.32 x (I) where x is the egg diameter
in /t. The correlation
coefficient
is 0.95.
Size of eggs of the genus Cu/mus Species
Size with standard error (,u)
Reference
Culanus jinmurchicus
145 163.9 :L 0.866 178.63 2.5 190 ’
Marshall & Orr ( 1953) Present worli McLaren (1966) McLaren et rrl. (I 969)
C. helgolandicus C. glacialis C. hyperboreus
’ Only one egg was measured.
DISCUSSION
The larger eggs of C. hyperboreus and C. glacialis take longer to develop than the smaller eggs of C.jinmarchicus and C. helgolandicus, i.e. the value of a in Belehradek’s equation is positively related to egg diameter (equation 1). Since a and b are known for an egg of given size (equation 1 and Table II), one can determine a by measuring the development time D at one temperature T and using Belehradek’s equation. This will be sufficient to predict the development time D for any other temperature T. A possible explanation for the linear relationship between development time corrected for differences in a (equation 1) is that development rate is determined by the surface : volume ratio which decreases with increasing diameter. One could think that the metabolic exchange between the egg and its external environment is relatively slower for the larger eggs with their relatively smaller sraface. Alternatively, one might assume that the development rate is determined by metabolic processes related to the size of the internal surfaces which in turn is proportional to the external surface. The value of a (which is often called the biological zero and is the theoretical temperature at which development is infinitely long) seems to be related to the geographical range of the species and presumably, therefore, to water temperature. Distributions of the species are given by Matthews (1969), Colebrook (1964) and Colebrook, GIover & Robinson (1961). Under the classification given by Colebrook, Glover & Robinson (1961) the distribution would be as follows: C. glacialis and C. hyperboreus - northern oceanic (a z - 8.5 “C), C. jinmarchicus - northern intermediate (CI = - 6.7 “C), C. helgolandicus - southern intermediate (a = - 4.9 “C).
DEVELOPMENT RATE OF COPEPOD EGGS
175
ACKNOWLEDGEMENTS
I should like to thank Dr R. P. Harris for his assistance during this work and Drs H. Meves and I. A. McLaren for reading the manuscript and making helpful suggestions. Mr D. K. Grif5ths and Mrs Helen Egginton assisted with the operation of the computer programmes. This work was carried out while the author was on a Fellowship from N.E.R.C. REFERENCES
BELEHRADEK, J., 1935. Temperature and living matter. Protoplasma Monographia, No. 8, Borntraeger, Berlin, 277 pp. BERRILL,N. J., 1935. Studies in tunicate development. Part III. Differential retardation and acceleration. Phil. Trans. R. Sot. Ser. B, Vol. 225, pp. 255-326. COLEBROOK,J. M., 1964. Continuous plankton records: a principal component analysis of the geographical distribution of zooplankton. Bull. mar. Ecol., Vol. 6, pp. 78-100. COLEBROOK, J. M., R. S. GLOVER& G. A. ROBINSON,1961. Continuous plankton atlas of the northeastern Atlantic and the North Sea. Bull. mar. Ecol., Vol. 5, pp. 67-80. CONOVER,R. I., 1967. Reproductive cycle, early development and fecundity in laboratory populations of the copepod Calanus hyperboreus. Crustaceana, Vol. 13, pp. 61-72. CORKETT,C. J., 1970. Techniques for breeding and rearing marine calanoid copepods. Helgoliinder wiss. Meeresunters., Bd 20, S. 318-324. CORKETT,C. J. & I. A. MCLAREN, 1970. Relationships between development rate of eggs and older stages of copepods. J. mar. biol. Ass. U.K., Vol. 50, pp. 161-168. DANNEVIG,H., 1895. The influence of temperature on the development of the eggs of fishes. Rep. Fishery Bd Scotl., 1894, Part 3, pp. 147-152. MARSHALL,S. M. & A. P. ORR, 1953. Calanusfinmarchicus: egg production and egg development in Tromse Sound in spring. Acta Boreal., A. Sci., Vol. 5, pp. 1-21. MATTHEWS,J. B. L., 1969. Continuous plankton records: the geographical and seasonal distribution of Calanusfinmarchicus s. 1. in the North Atlantic. Bull. mar. Ecol., Vol. 6, pp. 251-273. MCLAREN, I. A., 1966. Predicting development rate of copepod eggs. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 131, pp. 457-469. MCLAREN, I. A., D. A. WALKER& C. J. CORKETT,1968. Eflects of salinity on mortality and development rate of eggs of the copepod Pseudocalanus minutus. Can. J. Zool., Vol. 46, pp. 1267-1269. MCLAREN, 1. A., C. J. CORKETT& E. J. ZILLIOUX, 1969. Temperature adaptations of copepod eggs from the Arctic to the Tropics. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 137, pp. 486493.