Population dynamics of Tisbe holothuriae (Copepoda; Harpacticoida) in exploited mass cultures

Netherlands Journal of Sea Research 16:208-216 (1982)

POPULATION DYNAMICS OF TISBE HOLOTHURIAE (COPEPODA; HARPACTICOIDA) IN E X P L O I T E D MASS CULTURES by R. GAUDY and J. P. GUERIN Laboratoire d'Hydrobiologie marine, Faculte"des Sciences de Luminy, 70 Route Lgon Lachamp, 13288 Marseille Cedex 9, France

CONTENTS I. Introduction . . . . . . . . . . . . . . . . . . . II. Material and Methods . . . . . . . . . . . . . . . III. Results . . . . . . . . . . . . . . . . . . . . . A. Effectson population variables . . . . . . . . . . . . . . . . . B. Effectson population growth rate . . . . . . . . . . . . . . . . IV. Discussion . . . . . . . . . . . . . . . . . . . . V. Summary . . . . . . . . . . . . . . . . . . . . VI. References . . . . . . . . . . . . . . . . . . . .

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

208 209 210 210 213 214 215 216

I. INTRODUCTION Harpacticoid copepods belonging to the genus Tisbe constitute a suitable material to study optimum productions under controlled conditions, because of their rapid life cycle, a high reproductive potential and good resistance under experimental conditions where space limitation, lack of food and accumulation of metabolic products could possibly interfere with the production rate. Regular exploitation of these cultures for aquaculture purposes acts on the biomass and the production of the population. Thus a precise knowledge of the most adequate conditions of exploitation is needed to guarantee the maintenance of a good yield. The effect of external factors (temperature, salinity, food) on the classic population variables, intrinsic growth rate (rm) in particular, is now well known from experiments on isolated females of Tisbe and on their offspring, under conditions where space does not appear to be a limiting factor (GAUDY et al., 1982). On the other hand, crowding effects have been investigated only recently in small volume experiments (some ml) (FAvA & CROTTI, 1979; FAVA & R~NGOt.I, 1979). In large volume experiments (600 1) ALESSIO (1974) obtained constant population densities in T. furcata during long periods of exploitation, but does not provide detailed information on population dynamics. To the

D Y N A M I C S OF T I S B E I N MASS C U L T U R E S

209

contrary, HOPPENHEIT (1975, 1976) reported detailed results about several factors acting on the dynamics of T. holothuriae populations bred in small volume mass cultures (200 ml) with a weekly exploitation at different rates. This research aspect is approached in this paper in a different way by (1) breeding in larger volumes (10 1) of aerated sea water, conditions nearer to those allowing an applied exploitation, (2) comparing 2 different harvest rythms, (3) attempting to interpretate observed population variations by means of birth rate and death rate calculation. II. MATERIAL AND METHODS The copepods were maintained in 10 1 tanks with aerated sea water (19 ° C; 38%0 salinity) and natural light. The animals were fed in excess a compound diet (Tetramin) every 2 days. Three populations were followed, each starting with 50 ovigerous females taken at random from a laboratory strain (this strain is regularly enriched with individuals from nature). Culture A grew undisturbed during 3 weeks and then was exploited weekly at a 50% rate yielding half of the tank volume after previous mixing and replenishing with new sea water (at one occasion the total tank volume was renewed to avoid a threatening extinction of the population after 5 harvests). Cultures B and C were exploited every 10 to 12 days, after an initial period of 18 days. In culture B the yield was obtained in the same way as for the A culture. In culture C, the whole population was sieved off and half of it was replaced in 10 1 of new sea water. For counting, the different larval stages were separated, using the descriptions of LOPEZ (1980) for the closely related species T. cucumariae. Naupliar stages in the A culture were counted separately using haematometric cells. In cultures B and C, the stages were counted together. The development of the population was assessed by (1) the instantaneous exponential growth rate r0, calculated from individual numbers n1 and n2 present in the culture in the successive harvests at times I1 and

t2: ro -

(In n2

In nl) (t2 -- tl)-1

and by (2) the calculated instantaneous growth rate re, the difference between the instantaneous birth rate and death rate. The instantaneous birth rate b is derived from the equation: b = In (1 + B)

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R. G A U D Y & J. P. G U E R I N

where B, the finite birth rate, is modified with respect to the formula of EDMONDSON, COMITA & ANDERSON (1954) to take into account the part of the adult population available for the production of living nauplii: B

--

co'ho's't

1

where co is number of eggs per sac, h is hatching rate of eggs, 0 is part of females being ovigerous, s is part of adults being females and t is the development time of the eggs. In the calculations, h and ! were fixed at 0.5 and 2.5, based on mean values obtained in previous experiments (HoPPENHEIT, 1976; GAUDY & GUERIN, unpublished results). The instantaneous death rate d is calculated from the decrease in number of successive larval stages during their growth to the following stage: d --

(ln h I --

In &)

(t 1 --

~2)

1

In the calculations, total duration of larval growth, from the first nauplius up to adult was assumed to be 6 days, and intermoult periods were supposed to be equal for all stages. As mortality rates appeared to be rather constant for all stages, a common mortality rate was obtained by calculating the regression line of In numbers over time using the least squares method. Also for adults, the mortality rate was supposed to be equal to that of the larval stages because of their relative frequency in the population and their longevity as estimated from separate experiments with cultures yielded from the mass culture (Table II). The regressions calculated, however, do not include values obtained for the adults. In several cases numbers of the first nauplius stage appeared to be underestimated, probably because of a comparatively shorter development time. III. RESULTS A. E F F E C T S

ON

POPULATION

VARIABLES

In the 3 series, yield increases with time until a maximum is reached at the third sampling and then decreases afterwards (Fig. 1). Mean production is highest in the most frequently harvested culture and also high in the culture where the medium is entirely renewed at each harvest. Population structure (proportion of nauplii and adults) shows rather limited variation during experiment A, fluctuates to a greater extent in culture C and fluctuates considerably in culture B. Nauplii's relative abundance is directly related to population density (means in culture A

DYNAMICS

OF

TISBE

IN

MASS

211

CULTURES

86.4% , in B 52'.3% a n d in C 5 8 . 6 % ) . Sex ratio, ovigerous rate and n u m b e r of eggs p e r sac show parallel or opposite variations, with different p a t t e r n s in the 3 cultures ( T a b l e I). A

% 1oo~

B

U

so ~ 0

°°t

t~

~0 ~

] ~-

~___~

c

0

50 0

numbers ml -~

t

25 0

,

0

,

IO

,

20

,

,

30

40

°

,

50

o

i~

2o

3o

4o

so

6o

7o

~

,~o

2'o 3'0 4', s'0 6~ 7~ Oays

Fig. 1. Measurements in successive harvests from mass cultures (10 1 tanks) of Tisbe holothuriae; culture A with weekly exploitation and 50% water renewal; culture B with 10 to 12 days between harvests and 50°,'o water renewal; culture C with 10 to 12 days between harvests and 100% renewal (arrows indicate complete change of medium in A and salinity disturbance in C). a. Number of eggs per sac. b. Ovigariousness (° o tkmales with egg sacs!, c. Sex ratio (% females of adults), d. Naupliar proportion (~?o). e. Yield (numbers" ml 1). I n culture A, sex ratio shows reduced values d u r i n g several harvests and then increases acutely after the c o m p l e t e renewal of the sea water. O v i g e r o u s rate shows an opposite trend. T h e n u m b e r of eggs per sac decreases with time. I n culture B, sex ratio decreases sharply d u r i n g the last 3 harvests. O v i g e r o u s rate and eggs p e r sac v a r y in parallel, b o t h showing opposite fluctuations to those of sex ratio d u r i n g most of the time. I n culture C, sex ratio is reduced at the fifth sampling. T h i s reduction follows an a c c i d e n t a l decrease in sea w a t e r salinity (from 38 to 30~oo) tor a short time resulting f r o m a mistake d u r i n g the c h a n g i n g of sea water. O v i g e r o u s rate is r a t h e r stable, b u t the n u m b e r of eggs p e r sac shows considerable fluctuations, its m a x i m u m c o r r e s p o n d i n g to a m i n i m u m in the p r o p o r t i o n of females present. I t a p p e a r s f r o m the cultures t h a t variations in sex ratio, ovigerous rate a n d n u m b e r of eggs p e r sac contribute to a stabilization of the egg p r o d u c t i o n per adult (homeostatic

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212

TABLE

I

Number of eggs per sac (o9), ovigerous females proportion (o), sex ratio (% females) (s) and instantaneous birth rate (b) of Tisbe holothuriae for successive harvests in the cultures A, with high exploitation frequency; B, with low exploitation frequency and 50% medium renewal; and C with low exploitation frequency and 100% medium renewal. Harvest

1 2 3 4 5 6 7 8 mean

Culture A

Culture B

Culture C

co

o

s

b

co

o

s

b

co

o

s

b

37.00 39.80 42.20 34.80 28.45 32.50 17.92

62 62 56 75 56 38 53

22 33 30 30 27 53 42

0.698 0.966 0.883 0.942 0.621 0.837 0.587

33.20

57

34 0.791

40.42 39.57 34.00 12.08 24.92 33.20 25.50 33.23 30.37

46 40 50 8 11 75 28 50 31

65 59 36 63 56 22 14 14 41

1.229 1.054 0.799 0.115 0.268 0.740 0.182 0.382 0.596

63.50 45.08 30.00 28.08 131.00 75.00 52.60 24.49 43.60

40 42 52 33 42 37 58 28 40

71 49 50 50 32 17 29 29 35

1.528 1.049 0.940 0.656 0.607 0.671 1.019 0.333 0.850

ett~ct). C o n s i d e r i n g t h e sex r a t i o v a r i a t i o n s , t h e v a r i a b l e s a l l o w i n g t h e h i g h e s t c o m p e n s a t o r y effect a r e different. I n c u l t u r e A , t h e o v i g e r o u s r a t e p l a y s t h e m e a n p a r t , in c u l t u r e B o v i g e r o u s r a t e acts .jointly w i t h t h e n u m b e r o f eggs p e r sac. I n c u l t u r e C, t h e n u m b e r o f eggs p e r sac c o u n t e r b a l a n c e s sex r a t i o c h a n g e s . A s t h e q u a l i t y o f t h e c u l t u r e m e d i u m will d e p e n d g r e a t l y o n its r a t e o f r e n e w a l , it is p o s s i b l e t h a t d i f f e r e n c e s o b s e r v e d in p o p u l a t i o n d y n a m i c s o f c u l t u r e s a r e r e l a t e d to d i f f e r e n c e s in q u a l i t y o f sea w a t e r . T o c o n t r i b u t e to this p r o b l e m , a c o m p l e m e n t a r y e x p e r i m e n t w a s c a r r i e d out. O v i g e r o u s f e m a l e s f r o m n a t u r e w e r e i s o l a t e d in 50 m l f i n g e r - b o w l s , o n e set ( c o n t r o l ) w a s b r e d in fresh s e a w a t e r , t h e o t h e r in w a t e r c o m i n g f r o m a m a s s c u l t u r e ( T a b l e I I ) . I n t h e l a t t e r set, d e c r e a s e s w e r e o b s e r v e d in TABLE

II

Effect of the quality of medium water (fresh medium as control compared to medium already used for mass culturing) on the population dynamics of Tisbe holothuriae females (longevity of adults) and of their progeny (minimum generation time, number of adults produced, sex ratio of adults produced, and eggs per sac in the first sac of females produced) ; mean values with standard deviation. Medium

Control Test

Longevity (days)

Minimum generation time (days)

Number o f adults

Sex ratio

Eggs per sac

17.25 ± 3.78 11.14 ± 0.37 40.30 ± 5.20 0.39 ~_ 0.04 72.74 ± 0.71 12.82 ± 1.44 13.82 ~: 0.31 35.21 ± 3.18 0.12 -~ 0.03 53.33 ~ 1.79

DYNAMICS OF TISBE IN MASS CULTURES

213

their longevity ( 1 4 % ) , and in a b u n d a n c e (21 °/o), sex ratio (proportion of females) and eggs per sac p r o d u c t i o n (26%) of their progeny. O n the contrary, the m i n i m u m generation time (from egg to egg) was prolonged (22.5%). All these shifts c o n t r i b u t e to a lowering of the growth capacity o f the population, a result similar to that observed in mass cultures w h e n harvesting is less frequent or sea water renewal less complete. So the change in most o f the p o p u l a t i o n variables during the experiments can p r o b a b l y be related to the formation of a substance p r o d u c e d by the animals and a c c u m u l a t e d in the medium. B. EFFECTS ON POPULATION GROWTH RATE M e a n instantaneous birth rate values (b) are highest in culture C as the n u m b e r of eggs per sac is significantly higher t h a n in the cultures A and B (Table I). In culture B the lowest m e a n value of b is found because a somewhat elevated sex ratio is insufficient to balance the low values in ovigerous rate and in n u m b e r of eggs per sac. T h e birth rate in culture A is close to that in culture C because of a high p r o p o r t i o n ofovigerous females. Obviously a certain birth rate level can result from different m u t u a l combinations of the variables calculated during the experiments, e.g. a more frequent harvesting favours the ovigerous rate and an increased renewal of the sea water m e d i u m results in an increase in the n u m b e r of eggs p a r sac. T h e mortality rate ( - - d ) has been calculated only tor culture A, the one where the nauplius stages were counted separately. T h e mortality numbers

i-1 22V

27.V

3 VI

10000 -

I00 -

I

[

I

I

I

I

I

t

I

I

I

I

I

I

I

I

I

L

I

1

I

Oa~,s

I

I

Fig. 2. Numbers of successive larval stages versus time in culture A at dates of harvesting (indicated by • and • at alternating harvests; regression lines per date show instantaneous mortality rates (as durations of stages are assumed to be equal).

214

R. GAUDY & J. P. GUERIN

shows a tendency to increase regularly with time suggesting increased toxicity of the medium (Fig. 2). This is supported by the acute decrease in mortality following the total renewal of the sea water after the 5th harvest, and the renewed increase of mortality after the following 18 days without exploitation or water renewal (Fig. 3a). The calculated instantaneous growth rate of the population is almost zero at the tirst and the last sampling of the experiment when after a period of more than 18 days without exploitation the population can be supposed to be in steady sate (b -- --d). Comparison between r c and the observed rate r0 shows good agreement during the greater part of the experiment, but in the period between the 5th and the 6th harvest the observed value of nearly 0 contrasts with the very low and the very high calculated values tbr these harvest (Fig. 3b). The low one results from the joint effect of a lowered b and an increased d; the highest is the consequency of the acute reduction of --d following the total water renewal. Indeed, r0 corresponds to the average population growth between 2 harvests, whereas rc is calculated at each sampling time. b -el

Q.6 0.4

0.8

/"

02

O.6

"~ "~

0.4

/""

0.2

0 02 -04

lO

2tO 3~1] 4to 50 ~ays

Fig. 3. Population variables during the exploitation period of culture A. a. Instantaneous birth rate (0) and instantaneous death rate (at), b. Calculated (0) and observed (at) instantaneous growth rate (r).

IV. D I S C U S S I O N The numbers produced in the described, exploited cultures of Tisbe holothuriae are higher than obtained in small-volume, non-aerated cultures under similar conditions of exploitation (weekly harvesting at a 50% rate) by HOPPENHEIT (1975) and also higher than in larger volumes (but in different conditions of exploitation; daily harvests at a 40°~) rate) with T. furcata by ALESSlO (1974). Yields are larger at more frequent harvestings. Similarly, in MARSHALL'Sexperiments with Daphnia (1967), yields increased with the increase of harvest frequency until a maximum and then decreased. HEINLE (1970) found a decrease of yield in Acartia tonsa cultures with the increase of exploitation frequency and supposed that a frequency of 4 days was too rapid to maintain the

D Y N A M I C S OF T I S B E IN MASS C U L T U R E S

215

population level. In Tisbe holothuriae experiments the maximum yield was probably not reached as in the closely related species T. furcata, ALESSIO (1974) found no decrease in yield with daily harvests at a 40% rate for long periods of exploitation. Fluctuations in abundance are often noted in this type of experiments as resulting fi"om variations in birth and death rates related to the in vitro conditions, which are not always understood. In the present experiments also sex ratio and the numbers of eggs per sac appear to vary as they react to favouring factors as the renewal of the sea water or disturbing factors as the temporary decrease in salinity. A salinity effect on the population dynamics of T. holothuriae has been stated previously (GAUDY et al., 1982). Considering the different regimes in the 3 cultures, the quality of the culture medium has been emphasized. FAVA & CROTTI (1979) and FAVA & RINGOLI (1979) have shown that crowding resulted in a lowering of the nauplii production in T. holothuriae and in a decrease of survival rate during larval growth in 7-. clodiensis. These authors hypothesized the production of a chemical complex that modifies population variables resulting in a homeostatic effect. Similarly, HOPPENHEIT (1975) supposed the existence of an "imprinting" factor in T. holothuriae regulating the sex ratio of female's progeny in mass cultures. Our results support these assumptions. Considering the finale decrease of the population, the harmful effect of inbreeding does not seem to play an important part as the inbreeding rate is reduced by the start of the population with 50 females (taken at random) and by the large population density where crossings between parents in direct filiation are improbable. There is however another factor that will have been harmful for the populations in the cultures. It appears that the last harvests from the 3 cultures contained individuals of 2 other species, an undetermined harpacticoid copepod and an archiannelid, Dinophilus sp., species frequently found in polluted areas. The latter species often appears as the cause of extinctions of experimental cultures, and it is possible that it acts as a competitor in older cultures of Tisbe. V. SUMMARY Three cultures of Tisbe holothuriae in 10 1 tanks were harvested each 7 or 10 to 12 days at a rate of 50°/o . The most frequently harvested culture showed the highest yield. At lower exploitation rates a higher rate of sea water renewal resulted in a higher production. In the cultures, variations in sex ratio, ovigerous rate, and number of eggs per sac contributed to a stabilization of the egg production. More frequent harvesting favoured the ovigerous rate and

216

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a h i g h e r r e n e w a l r a t e o f the m e d i u m resulted in m o r e eggs p e r sac. T h e g r o w t h r a t e o f t h e p o p u l a t i o n was e s t i m a t e d f r o m c a l c u l a t e d values for b i r t h r a t e a n d d e a t h rate, a n d this estimate was c o m p a r e d w i t h t h e o b s e r v e d g r o w t h rate. T h e q u a l i t y o f the sea w a t e r m e d i u m in mass cultures was investig a t e d a n d discussed in its effects o n p o p u l a t i o n d y n a m i c s . VI. RFERENCES ALESSIO,G., 1974. Riproduzione artificiale di orata Sparus aurata (L.) (Osteichtihyes, Sparidae) 3~. Produzione su vasta scala di fito e zooplancton per l'alimentazione della larve e degli avannoti.--Boll. Pesca Piscic. Idrobiol. 29:133-147. EDMONDSON,W. T., G. F. COMITA& G. C. ANDERSON, 1954. Reproductive rate of copepods in nature and its relation to phytoplankton population. Ecology '13: 625~534. FAVA,G. & E. CROTTI,1979. Effect of crowding on nauplii production during mating time in Tisbe clodiensis and T. holothuriae (C.H.).~elgol~nder wiss. Meeresunters. 32: 466~475. FAVA, G. & C. RINaOLI, 1979. Sopravivenza da nauplio ad adulto a diverse gradi di affollamento, nella specie polimorfa Tisbe clodiensis (Copepoda, Harpacticoida). Areho Oceanogr. Limnol. 19" 157 167. GAUDY,R., J. P. GUERIN & M.'MORAITOUAPOSTOLOPOULOU,1982. Effect of temperature and salinity on the population dynamics of Tisbe holothuriae, Humes (Copepoda; Harpacticoida) fed two different d i e t s . ~ , exp. mar. Biol. Ecol. 57: 257-271. HEINLE, D. R., 1970. Population dynamics of exploited cultures of calanoid copepods.~Helgol~.nder wiss. Meeresunters. 20: 366-372. HOPr'ENHEIT, M., 1975. Zur Dynamik exploitierten Populationen von 75sbe holothuriae (Copepoda, Harpacticoida). II. Populationsdichte, Alterzusammensetzung, Wachstum und Ausbeute.--Helgol~inder wiss. Meeresunters. 27" 377-395. , 1976, Zur Dynamik exploitierten Populationen von Tisbe holothuriae (Copepoda, Harpacticoida). III Reproduktion, Geschlechtsverh~iltnis, Entwicklungsdauer und l~berlebenszeit.--Helgolander wiss. Meeresunters. 211:109 137. LovEz, G. W., 1980. Description of the larval stages of Tisbe cucumariae (Copepoda: Harpacticoida) and comparative development within the genus Tisbe. -Mar. Biol. 57: 61-71. MARSHALL,J. B., 1967. Radiation stress in exploited Daphnia populations. ~Amnol. Oceanogr. 12: 154-158.