Canadian Translation of Fisheries and Aquatic Sciences No. 5047

ISSN 0704-3716

Canadian Translation of Fisheries and Aquatic Sciences

No. 5047

Changes in motor activity and fat consumption in Acartia clausi Giesbr. during long fasting

T.M. Kovaleva, and N.V. Shadrin

Original title: Izmenenie dvigatel l noi aktivnosti i raskhod zhira u Acartia clausi Giesbr. pri dlitel'nom golodanii

In: Ekol. Morya (14): 44-50, 1983

Original language: Russian

Available from: Canada Institute for Scientific and Technical Information National Research Council Ottawa, Ontario, Canada R1A 0S2

1984

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LIBRARY IDENTIFICATION - FICHE SIGNALÉTIQUE TrA-s 5041 Translated from - Traduction de Into - En Russian English Author - Auteur Kovaleva, T.M., and Shadrin, N.V.

Title in English or French - Titre anglais ou français Changes in motor activity and fat consumption in Acartia Clausi Giesbr. during long fasting

Title in foreign language (Transliterate foreign characters) Titre en langue étrangère (Transcrire en caractères romains) Izmenenie dvigatel'noi aktivnosti i raskhod zhira u Acartia Clausi Giesbr. pri dlitel'nom golodanii

Reference in foreign language (Name of book or publication) in full, transliterate foreign characters. Référence en langue étrangère (Nom du livre ou publication), au complet, transcrire en caractères romains.

Ekologiya morya

Reference in English or French - Référence en anglais ou français

Ecology of the Sea

Publisher - Editeur Page Numbers in original A.O. Kovalevskii DATE OF PUBLICATION Numéros des pages dans Institute of Biology of the South DATE DE PUBLICATION l'original Seas, Academy of Sciences of the 44-50 Year Issue No. Volume Place of Publicati Pcrei-Tri-an—S-S.R Année Numéro Number of typed pages Lieu de publication Nombre de pages dactylographiées Kiev, USSR 1983 14 18

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Source: Ekologiya morya (Ecology of the Sea), No. 14, 1983, pp.44-50, published by the A.O. Kovalevskii Institute of Biology of the South Seas, Academy of Sciences of the Ukrainian SSR, "Naukova dumka" press, Kiev. Changes in Motor Activity and Fat Consumption in Acartia Clausi Giesbr. During Long Fasting

T.M. Kovaleva and N.V. Shadrin U.D.C. 591.13 * In natural bodies of water, both in time and in space 44 the distribution of the items sought for food is character- ised by great variability. During certain periods of time and in certain sections of a water area, the concentration of food can decrease almost to zero. In such cases the animals fast. A result of the fasting, on which V.S. Ivlev was the first to focus attention clearly [1], is a change in the behaviour of the animal, in its resistance to the effects of various biotic and abiotic factors. When constructing models of natural ecosystems it is necessary to take into account both the considerable variability in the adequacy of the food supply, both in space and in time, and the reactions of animals of all

The figures in the right-hand margin are the page numbers of the original (Tr.).

SEC 5-25 (Rev, 82/1 1 ) Canadâ trophic levels to the variable length of fasting. There are now a number of published studies which show the effect of long fasting on certain characteristics of copepods (in particular, the respiration rate of copepods decreases when fasting [8,9 et al]). When maintained for two months in a foodless environment the rate of respiration in Calanus cristatus underwent a twofold decrease, while in A. clausi and A. tonsa, during a six- day fast, the rate of respiration fell to one half and one third of the initial values [8]. In fasting copepods a decrease in excretion of ammonia and inorganic phosphorus is also seen [8,9]. The quantitative characteristics of the daily loss in mass exhibit significant differences in the various species. This is on account of the differing mobility and biochemical peculiarities of small crustaceans. During a 24-hour fast, Calanus plumchrus loses 1% of body mass, Acartia clausi 6% and A. longiremis, between 1.5 and 10% [8]. In fasting copepods, the quantitative relation between proteins, fats and hydrocarbons may change. In certain of the species possessing substantial reserves of fat, at the outset of fasting it is principally the fat that is utilised. Thus, in Calanus helgolandicus when maintained in clean water without food, after five days there was a twofold decrease in the quantity of lipids [11], 3

whereas the decrease in proteins and nitrogen was only slight [9]. In animals of the Acartia type which are furnished with a small quantity of fat, the proteins are actively metabolised from the outset of fasting. These and other differences result in the fact that the survival time during fasting amounts to two or three days in some copepod species, and can be up to two months and more in others [7-10 et seq.]. Fasting affects not only the metabolism of planktonic crustaceans but also their behaviour. During a short fast, some increase in the motor activity of copepods was seen [5]. When copepods were kept without food for long periods a marked decrease in their motor activity was observed [3]. Overall, it is important to note that the effect of fasting on the behaviour, metabolism and mortality of copepods has hardly been studied at all. It was for this reason that we conducted research on a highly abundant species of Black Sea zooplankton: Acartia clausi Giesbr. We traced the effect of fasting on motor activity, the rate of consumption of fat droplets and the survival time. Material and methodology. In studying the behaviour of the A. clausi copepods we set ourselves the task of quantitatively evaluating certain characteristics of their behaviour in a fobdless environment. For this 4

purpose the small_crustaceans were caught with a Juday net furnished with a No. 23 fine mesh, in a 10-mile zone of the Black Sea near Sevastopol. In the laboratory, the planktonic animals selected from the sampling (average size of females 1.2mm) were placed singly in half-liter flasks containing water that had been passed through a No. 3 membranous filter. The water temperature was 18-19 °C. Food consisting of Peridinium trochoideum In a concentration of 3g/m3 was added to the control flask. The experiments lasted 6-7 days. In all, 10 experiments were performed. According to the data of T.S. Petipa [6], in A. clausi the highest rate of food consumption and the maximum speed of searching for it is observed during the period 8-11 hours. During the second half of the day (13-16 hours) less active feeding and a lower mean rate of movement are seen. In view of this, we monitored the behaviour of the planktonic animals over a 10-hour period. The following behavioural parameters were determined: 1 (1) the number of segments of rowing movement (between stops) per unit of time, min-1 ; (2) the duration of the pause; (3) the length of the "jump", mm; the extent of the segments of rowing moement between stops.

1According to the new terminology [6], a "large jump" is more correctly referred to as rowing, since this is an elementary or compound rowing motion. 5

The time parameters were measured with a stopwatch. The length of the "jump" was determined by using a micro- meter-eyepiece positioned beneath a MBS-1 binocular. The crustaceans were placed in hemispherical flat-bottomed cups and were observed through the binocular, the lens of which was rigidly attached to the stand, thus affording an opportunity of moving the lens in various directions without frightening the animal. Long segments of rowing movement were measured with a millimeter rule, for which purpose the cup containing the Acartia was covered with glass measuring 12 x 9 cm and with a thickness of 1.5mm. Using a fine drafting pen and India ink, dots marking the initial position of the crustacean when at rest and its position after completing a "large jump" were then plotted, and the trajectory of the path was drawn and measured. Additionally, the speed of submergence of the planktonic animals was determined in the half-liter flasks. This value was derived by recording the travelling time (6-184 sec) of the crustacean along the vertical in the 0.3-10cm region. A further 10 experiments were performed in order to determine fat droplet consumption during fasting (the females were placed singly in 100m1 of water without food). The crustaceans were fished out daily and in a small drop 6

of water under a MBI-3 microscope measurements were obtained of the thickness, width and length of the fat droplets. The crustaceans were then transferred to a new flask in which the former conditions were present. In determining the mass of the fat droplets their shape was equated to the appropriate geometric figure (as a rule, a sphere or spheroid) and their volume was found from the equations V1 -4/3nle, (1)

where R is the radius of the sphere

V2 __413 abc, (2) and where a,b,c are the semiaxes of the ellipsoid. The mass, expressed in mg, was determined from the calculated volume and specific gravity of the fat; the latter was taken to be 0.91. Each mean parameter was found from 10-30 measurements (in all, 2040 of them were completed). All of the numerical data were processed by the methods of variational statistics. Results. After being fished from the sea and transferred to clean water, the copepods were at first very restless, travelling by means of large, rapid "jumps". Gradually they became more quiescent and after 30-60 minutes, locomotion was accomplished by small "jumps", the mean length of which was 1.78-3.79mm (2.614.40 mm on the average). There were few massive "jumps" of 19.0±2.5mm. The antennae, abdomen and thoracic limbs participate in the act of motion, the principal role being played by the thoracic limbs [6]. With fasting and the resulting overall decrease in the number of "jumps" per unit of time, the number of large "jumps" increased, reaching a peak by the third day. Thus, whereas on the first day of fasting the proportion of "large jumps" in the total number of movements amounted to 107e , on the second day it was 16% and on the third, 28%. Thereafter the number of large "jumps" declined and at the end of the experiment the crustaceans were only executing small "jumps". It is noteworthy that on the second day'of fasting, Acartia did not only execute "jumps" in a straight line. In some cases, the route travelled assumed an arched or zigzag configuration owing to the work of the abdomen, which fulfills the role of a rudder. Beginning on the fourth day of fasting the copepod moved only in a straight line, upwards, downwards and sideways. After a series of "jumps" there follows a period of rest. The relation between the number of. "jumps" and the number of pauses varies with time. On the first day of fasting it equalled 1.5, by the fourth day it had risen to 2.5, and on the last day it dropped to 1. Motor activity 8

gradually diminished with an increase in the length of the pauses. During the resting period the animal may be oriented upwards, downwards and towards the head. It is as if the crustacean is "expiring", for it continues working the oral extremities for some time and then slowly sinks into the water until the next "jump". In spite of the feeble activity manifested at the end of the fast, the reaction of copepods to avoid danger is preserved until the last days of life, as evidenced by the "jump" response to the approach of a dissecting needle or pipette. Except for the first day of the fast, the copepod stayed on the less illuminated side at a distance of

2-15 cm from the bottom. On the last day of life it frequently lay on the bottom of the flask, which is indicative of the animal having become completely exhausted and thus incapable of resisting the tendency to sink. Similarly, it is typical of the behaviour of Acartia when maintaining it without food for there to be no glides. The animal travels by means of "jumps". In en environment where food is present, besides the "jumps" an Acartia also uses glides for locomotion. Glides account for between

0.8 and 16.6% of the total number of movements. It is interesting that the more intensively the animal feeds, the greater is the proportion of glides to the total number of movements. In Acartia, there is an absence of long "jumps" when searching for food. The length of a short "jump" by an Acartia amounts to 2.96-0.16+ mm, and that of a glide, to between 0.18 and 0.37 mm. The quantitative characteristics of the behaviour of the copepods are represented in figs. 1 and 2. As will be seen from fig. 1, during long fasting (6-7 days) the motor activity of the animals decreases. On day 1 of the observations the Acartia were active and completed 39-63 "jumps" per minute. With continued presence of the animals in the foodless flasks the number of "jumps" diminished. A sharp decline in the frequency of the "jumps" was observed by day 4, when in relation to day 1 the frequency of them had contracted by 92%, and on day 6, by more than 99%, or 200.fold. The number of "jumps" decreased as the length of the pauses increased (fig. 2). At the outset of fasting the pauses were short and their duration ranged from 0.83 to 2.12 sec. On subsequent days, as will be seen from fig. 2, the duration of the pauses increased 1.8-5.8 times relative to that of the preceding days. There were abrupt changes in the duration of the pauses beginning with the fourth day of fasting, when the length of the resting periods increased 28 times in comparison with the first days, amounting to 40 sec on the average. 10

On the sixth-seventh day the length of the pauses was numbered in minutes, that is, it had increased 142-294 times in comparison with day 1. Presumably, at the beginning of fasting the copepods are moving in order to search for food, while it is probable that subsequently, the movements are chiefly for the purpose of maintaining the body in suspension. In the course of the pauses the copepods sink at a mean speed of 19.8±2.0 mm/min. According to our calculation, beginning on the third day of fasting the animals could sink 27-28 m/day. During the five subsequent days of fasting the total descent can be as much as 140 m, unless one takes into account the effect of the water density on the animals rate of submergence, since the former increases with depth. The small number of observations that we made on the rate of submergence of dead Acartia gave values 200% greater than those for live animals.

Fig. 1. Change in the number of "jumps" per unit of time in A. clausi during long fasting. 11

As already noted, long fasting of planktonic animais is accompanied by consumption of the biochemical substrates. Serving as confirmation of this were our observations of the change in the inass of droplet fat in the bodies of the crustaceans.- Prior to fasting, from one to four spherical droplets measuring 11.4-68.4 microns were counted in each individual. Their total mass calculated per crustacean averaged 2.9 X10 -5 ± 1.4X10-5 mg, that is, 0.058% of the wet mass of the body. On the second day of fasting the mass of the fat droplets in a crustacean was 0.91X10-5 mg, on the third day, 0.04X10 -5 mg, and by the fourth day the fat droplets had been completely consumed (fig. 3). It was noted that in females with formed eggs there were fewer fat droplets (0.57X10-5 ± 0.10X10-5 mg, or 0.01% of the wet mass of the body) than in individuals in which egg formation had only just begun (1 or 2 partly formed eggs). The mass of the fat droplets in such crustaceans was 5.32X10 -5 ± 2.46X10 -5 mg, or 0.11% of the wet mass of the body. In females without eggs the fat droplets had completely disappeared after two days, that is, the daily consumption of fat from the first to the second day of fasting was 0.07% and from the second to the third day, 0.0357, whereas in the females with eggs, 0.01-0.0002% of the wet mass of the body was consumed daily. It is 12

important to note that on the average, an Acartia loses 67 of the body mass during a 24-hour period of fasting [8], that is, as early as the first day of fasting, fat utilisation does not play a major role in the total metabolism, amounting to between several fractions of a percent and 10% of the total mass of the metabolised products. The rapid consumption of the biochemical substrates cannot fail to affect the survival time. It was noticed that death of the crustaceans began to occur on the second day of their presence in the foodless environment. Over a 5-day fast 50% of the crustaceans died. The maximum survival time of solitary individuals was 11-12 days. The varying survival time of the fasting crustaceans was due, in all probability, to individual peculiarities of the animals, including their differing physiological states. Discussion. Fasting has an effect on very diverse characteristics of the vital activity of an Acartia. In studying its effect on the behaviour of a crustacean it is important to note that, beginning with the first hours of fasting and continuing until death there are gradual changes in both the character of motor activity and in its intensity. The intensive activity of the crustaceans observed at the outset of fasting is probably associated with the search for food. At that time the crustacean 13

executes many small "jumps" which facilitate the detection of food. A lack of food results in the appearance of large segments of rowing motions, especially on the third day of fasting. By means of these, the copepods more rapidly find aggregations of food under natural conditions and are able to travel at a rate of 10-16.5 cm/sec and more [2,4,6].

5,0

0 P "0 4.0)

4-I •o-1 u)

Fig. 2. Change in the duration of the pauses in A. clausi during long fasting. Fig. 3. Fat consumption in A. clausi during fasting:(1) in individuals not containing partly formed eggs in their bodies, (2) in individuals with fully formed eggs, (3) at the mean value of fat consumption. 14

Thereafter, motor activity of the Acartia diminishes, the number of "jumps" decreases and the duration of the pauses increases. In studying the effect of fasting on the fry of fishes, Ivlev [1] found that during fasting there is an increase in the fatiguability of the fry and consequently, in the duration of the resting periods as well. In our experiments this is probably due to the fact that with exhaustion the fatiguability of the crustaceans increases and they require more time to recover their strength. Apparently, a decrease in motor activity during fasting is typical of animals of diverse taxonomie position. On the 6th-7th day, by which time a substantial part of the biochemical substrates is consumed, the animals travel only by small, infrequent "jumps", which probably accounts for the fact that submergence of the animal slows down. Even as early as the beginning of the third day, however, the crustaceans are in no condition to compensate by means of "jumps" for submergence during the pauses and they gradually sink into the deeper layers. The periods of motor activity and survival during fasting in A. clausi are of brief duration. With these indices of bathyplanktonic migrating species of copepods, the survival time of Acartia during fasting is 5-10 times less [7,8]. The content of fat droplets in the body of an Acartia does not exceed 0.11% of the wet mass of the body. This is much less than in the body of Calanus type copepods, where the content of fat droplets can exceed 177 of the wet mass of the body [6]. It is for this reason that from the outset of fasting in Acartia, structural proteins evidently begin to be utilised. The variable resistance to long fasting in different species of copepods represents an adaptation to the specific characteristics of the environment inhabited by the species in question. A. clausi, existing in a surface layer that is rich in nutrients, has a capability of satisfying its food requirements almost constantly. Accordingly, representatives of this species do not amass large reserves in the form of fat droplets and are incapable of enduring long fasting. Conclusions. 1. In a foodless environment A. clausi travels exclusively by means of "jumps". There are no glides. The mean length of the small segments of rowing motion ("jumps") is 2.61 ± 0.40 mm, and of the large segments, 19.0 ± 2.5 mm. The share of the large segments of rowing motion in the total number of them is 0-28%. Their highest percentage is noted on the third day of fasting; at the end of life they are almost non-existant. 2. During long fasting, motor activity decreases, as evidenced bY the contraction of the number of segments of 16

rowing motion "jumps" and the 200-fold and more increase in the length of the pauses as compared to the first day of the observations. 3. The mass of the fat droplets per female is on average 2.9X10-5 ± 1.4X10-5 mg, or 0.0587 of the wet mass of the body of the crustacean. During fasting a fat droplet is consumed after three days . . 4. A. clausi, inhabiting layers where there is a concentration of phytoplankton, does not amass large fat reserves and is incapable of enduring long fasting. 17

REFERENCES

1. Ivlev, V.S. Experimental Ecology in Relation to the Feeding of Fishes. - Moscow, "Nauka" press, 1955. 252pp. 2. Pavlova, E.V., and Tsareva, L.V. Movements of Calanus helgolandicus as derived from filming data. - Biologiya morya (Biology of the Sea), Kiev, 1975, No. 33, pp. 64-68. 3. Idem. Effect of starvation and the presence of food on the motor activity of Calanus helgolandicus Claus. - In: Distribution and Behaviour of Marine Plàfikton in Relation to the Microstructure of Waters. Kiev: "Nau- kova dumka" press, 1977, pp. 77-84. 4. Pavlova, E.V. Speed of movement of copepods from the plankton of the Indian Ocean. - Ekologiya morya (Ecology of the Sea), 1981, No. 5, pp. 61-65. 5. Petipa, T.S., and Ostrovskaya, N.A. Parameters of the trophic behaviour of marine copepods and a quantitative description of them. - In: Distribution and Behaviour of Marine Plankton in Relation to the Microstructure of Waters. Kiev: "Naukova dumka" press, 1977, pp. 45-57. 6. Petipa, T.S. The Trophodynamics of Copepods in Marine Plankton Communities. - Kiev: "Naukova dumka" press, 1981. 242 pp.

I. Ile.dee B. C. Bucnepumearanbnan nuouornn nnTanun pbt6. — M.: Harm, 1955. -- 252 c. 2. Ilcumosa E. B., flapesa JI. B. ilanucenue Calanus helgolandicus no Aannum KHHO- CbeHKH. — Buouornn mops. Knee, 1975, Bun. 33, c. 64-68. 3. Ilatmoea E. B., L(apena JI. B. Bniuunte roaoaa u nannnne man na nanrareAbwyto aKTIIRHOCTb Calanus helgolandicus Claus. — B Pacupeae.nenne n noriezenne mop- ocoro naanuroua B CHS311 c unnpocrpperypoll acta. Knell : Aymna, 1977,.c. 77— 84. 4. liaemosa E. B. Cuopocrb naioneunn uoneno.a na nnanurona liu.rualcuoro °Kean& — 31conornn mopn, 1981, man. 5, C. 61-65. 5. Hen= T. C., Ocrpooriccua H. A. Ilapamemme numeaoro noeeenun uopcxnx nonenoA Eo.nnnecTseunoe onncamue. — B Kn.: Pacapeaezeinie n noaeaenne uopcicoro ITHHHIVIOH3 a c311311 c munpocrpyrrypoR noa. Knea Hayn. AymEca, 1977, c. 45-57. 6. Ileruna T. C. Tpocbonunannua uonenon n uopcuux nzamtronnux coo6ulecutax. — KT»: Harc. nymna, 1981. — 242 C. . • 18

7. Dagg M. Some effects of patchy food environments on copepods. — Limnol. and Oceanogr., 1977, 22, N 1, p. 99-107. 8. Ikeda T. Nutritional ecology of marine zoppleliztorl.._---Mem. _Fac.-.Fish.- Hokkaido - -. Univ., 1974, 22, N 1, p.• 1=97.-- 9. Ikeda T. The effect of laboratory conditions on the extrapolation of experimental measurements to the ecology of marine zooplankton. 4. Changes in respiration and excretion rates of boreal zooplankton species maintained nuder • ed and starved conditions. — Mar. Biol., 1977, 41, N 3, p. 241-252. • 10. Lilletund H., Lasker R. Laboratory studies of production by marine copepods fish Larve. — Fish. Bull., 1971, 69, N 3, p. 655-667. 11. Sargent L. R., Gotten R. R., Corner E. D., Kilvington L. C. On the nutrition and metabolism of zooplankton. XI. Lipids in Calanus helgolandicus grazing Buddulphia sinensis. — J. Mar. Biol. Assoc. U. K., 1977, 57, N 2, p. 525-533.

A.O. Kovalevskii Institute of Biology of the South Seas, Academy of Sciences of the Ukrainian SSR Received February 18, 1982

T. M. KOVALEVA. N. V. SHADRIN CHANGES IN MOTOR ACTIVITY AND FAT CONSUMPTION IN ACARTIA CLAUS1 G1ESBR. DURING LONG FASTING Summary Acartia clausi Giesbr. has been studied for its behaviour and fat consumption under long fasting. In foodless media Acartia clausi moves exceptionally due to rowing movements. The length of small portions of rowing movements between stops («jumps») is 2.61±0.40 mm, that of large ones is 19.0±2.5 mm. The number of «jumps» is found to decrease on the 6-7 th day of fasting. the pause duration increasing 200-fold and more, as compared with the first day of observation. Acartia clausi inhabiting phytoplankton-accumulated laj,ers have no large fat reserves as a fat drop in the animal body gets consumed for three days.