Physiological responses of adult Penaeus semisulcatus (de haan) to changes in salinity

Com;~.Biochem.Physiol. Vol. IOIA, No. 1,pp.117-119,1992

0300-9629/92 $5.00+ 0.00

Pergamon Press plc

Prinlzd in Great Britain

PHYSIOLOGICAL RESPONSES OF ADULT PENAEUS SEMISULCATUS (DE HAAN) TO CHANGES IN SALINITY J. V. CLARK* Department of Zoology, University of Kuwait, P.O. Box 5969 Safat, 13060 Kuwait (Received 3 December

1990)

Abstract-l.

Adult intermoult Penaeus semisulcatus were shown to be relatively poor osmoregulators. 2. They respond to 18O&salinity with a fall in respiration rate and death. 3. They have a narrow optimal survival range in salinity tolerance tests. 4. The slope of haemolymph concentration against seawater concentration was found to be 0.73, much higher than values reported for other species of the genus.

INTRODUCTION

Wcirk on shrimps of the genus Penaeus has shown tha: the degree of osmoregulatory capacity varies frown species to species (Bishop et al., 1980; Castillo am Lawrence, 1981; Dall, 1981; Dal1 and Smith, 19Z;l; Ferraris et al., 1986; Parado-Estepa et al., 19r;7). Adults are less euryhaline than the larvae, which are usually found in brackish water (Panikker, 1986; Castillo and Lawrence, 1981; Cawthorne et al., 1983). Penaeus semisulcatus is a commercially important shrimp found in Kuwaiti waters, the northern limits of whose fisheries coincide with a surface sal.nity of 36% (Mathews et al., 1979; Farmer and Uk awa, 1986). Larvae of P. semisulcatus, unlike other species of the genus have an optimum salinity of about 40% (Farmer et al., 1979) and are not found in brackish water (Drobysheva and Aseev, 1976; Al. Attar, 1979). I’resented here is some work on the response of P. sesxisulcntus adults to altered salinities, which can be rel tted to work on other penaeid species and to the distribution of the adults in Kuwaiti waters. MATERIALS AND

METHODS

Shl imps

r’kdult (20-70 g) P. semisulcatus obtained by trawling were supplied by the Kuwait Institute for Scientific Research. The animals were maintained at a salinity of 40°b in 200 1closed seawater aquarium systems and fed on raw shrimp flesh. 1ntl:rmoult animals were selected for the experiments and dala from those animals that moulted during the experimInts were not pooled with the rest. All experiments were carried out at 25-27°C. Re’,piration measurements

-hese were carried out in 3 1 respiration chambers, whose wa :er supply was cut off before the measurement period and resumed at the end (usually after 30-60min). Oxygen col~entrations were measured immediately before and after the period of interrupted water flow, during which the water surface in the respiration chambers was covered with a plastic sheet to prevent gas exchange. A respiration chamber *Present address: Academic Cardiology, St. Mary’s Hospital, London W2 1NY.

with no shrimp served as a control. Oxygen levels were measured with an Orion oxygen electrode (Model 97-08). Measurements were taken at 8 hr intervals, the shrimps being fed between readings. The first reading taken after an alteration in salinity was taken 30min after the change. After an experiment the shrimps were blotted dry and weighed so that oxygen measurements could be converted to units of milligrams of oxygen consumed per gram fresh weight of shrimp per hour. Salinity tolerance

To each of seven 13 1 tanks containing aerated sea water of different salinities (10, 20, 30, 40, 60, 70 and 80%) were added 10 shrimps. Mortalities were observed every 4 hr. Lower salinities were prepared by dilution with distilled water, and higher salinities by the addition of inorganic salts (Harrison et al., 1980). Haemolymph concentrations

Shrimps used in the salinity tolerance tests were sampled for haemolymph at 52 hr, with l-2 ml of haemolymph being withdrawn by syringe from the pericardial cavity. The samples were stored frozen. Later, osmolality of the thawed samples was measured using a Knauer Halbmikro osmometer. Successive freezings and thawings of a haemolymph sample showed that frozen storage did not significantly affect measured osmolality.

RESULTS

Respiratory rates

As might be expected, oxygen consumption of intermoult adult shrimps was inversely related to weight (Fig. 1). Two shrimps that moulted during the period of measurement showed a higher (average of 100%) respiration rate than the intermoult animals. Eflect of reduction of salinity

A reduction of salinity from 40 to 329/mhad no significant effect on respiratory rate (Fig. 2), but a greater reduction, from 40 to 18% resulted in a highly significant (P < 0.01 ANOVA) reduction in respiration rate (Fig. 3). At this time all the shrimps were moribund; by 12 hr after the salinity change all were dead. 117

118

J. V.

CLARK

Y zz 1,5x-O.5”

40%0

I

I I

8

16

,

20

30

40

50

60

I

I

32

40

I

0

18%.

I

24

Hours

70

Fig. 3. Respiratory response of shrimps (ordinate) to a change in salinity from 40°60to 18%. Each mean is of tive animals, and is shown with the standard deviation.

Shrimp weight(g) Fig. 1. Respiration rate (ordinate) against weight of adult intermoult shrimps kept at 40%0. The dotted line is a plot of the calculated relationship.

1800

Hours

Fig. 2. Respiratory response of shrimps (ordinate) to a change in salinity from 40%~to 3Z”%o. Each mean is of four animals. and is shown with the standard deviation.

6001

,

,, 600

Salinity tolerance

Hae~oly~p~

of adult shrimps at differin Table 1. The optimum for survival in these tests fell off more slowly for than for salinities above.

j

900 1200 1500 1800

Seawater

The percentage survival ent salinities is presented concentration of seawater was 40%0. The survival salinities below optimum

,

mOsmoles/kg

Fig. 4. Osmotic concentration of shrimp haemolymph (ordinate) against seawater concentration (abscissa). The solid line is drawn through the means of the data points. Calculated slope = 0.73. The dotted line is the isosmotic line. The two open circles are data from shrimps held at a salinity of 32% for 40 hr before transfer to 20%0.

concentrations

saiinity, and in the salinity tolerance tests there is high mortality of adult shrimps in a short period of time (52 hr) outside a salinity range of 30-60%0. The slope of haemolymph concentration against salinity (Fig. 4) has a high value (0.73), again suggesting poor osmoregulatory capacity. Nevertheless, by the definition of Lange (1972). Penaeus semisulcatus is a euryhaline organism in that it can tolerate salinity ranges of l&30%0 or more. Although P. semisulcatus has an isosmotic point (_ 3OS) similar to those reported for other species of the genus (MacFarland and Lee, 1963; Bishop et al., 1980; Dall, 1981; Cawthorne et al., 1983; Parrado-

The results of the experiments summarized in Fig. 4, show that the haemolymph of shrimps kept at 40%0 is hyposmotic to seawater, and that the isosmotic point is at about 930 mOsM, or a seawater concentration of 33%0. DISCUSSION

Three lines of evidence suggest that P. semisulcatus is a poor osmoregulator relative to other penaeid species. The fall in respiration rate and subsequent death when transferred from 40 to 18%~ (Fig. 3) indicates an inability to osmoregulate at the lower Table 1. Per cent mortality Test salinity (Y&s) 10 20 30 40 @3 70 80

with time of adult shrimps

held at different

salinities.

In each

case N = IO

Hours elapsed 4 IO 0 0 0 0 0 0

8

I2

!fj

20

24

28

32

36

40

44

48

5c

30 0 0 0 0 40 100

100 0 0 0 0 60 100

100 0 0 0 0 100 100

100 0 0 0 0 IO0 100

100 IO 10 0 0 loo loo

100 IO 10 0 0 100 100

100 40 10 0 0 100 100

100 80 IO 0 II loo 100

100 ;;

100 ;;

0 0 loo 100

0 IO loo loo

100 80 IO 0 IO 100 loo

100 80 10 0 10 100 100

Penaeus semisulcaius Table 2. Reported slope values of haemolymph against concentration for species of Penaeus

Penoeus species P. P. P. P. P. P. P. P. -.

svmisulcatus

a~lecus

duorarum St’tifero monodon itldicus usmnamei s: ylirostris

Slope 0.73 0.38 0.38 0.27 0.26

0.24 0.21 0.16

seawater

Source This paper Castillo and Lawrence (1981) Williams (I 960) Williams (1960) Ferraris et al. (1986) Parado-Estepa et ol. (1987) Williams (1960) Castillo and Lawrence (1981)

salinity responses

119

Bishop J. M., Gosslink J. and Stone J. (1980) Oxygen consumption and haemolymph osmolality of the brown shrimp, Penaeus aztecus. Fish Bull. 78, 741-757. Castillo F. Jr and Lawrence A. (1981) The effect of salinity on the osmotic, sodium and chloride concentrations in the haemolymph of euryhaline shrimps of the genus Penaeus. Comp. Biochem. Physiol. 68A, 75-80. Cawthorne D., Beard T., Davenport J. and Wickins J. F. (1983) Responses ofjuvenile Penaeus monodon (Fabricius) to natural and artificial seawaters of low salinity. Aquaculture 32, 165-174.

Dal1 W. (1981) Osmoregulatory ability and juvenile habitat preference in some Penaeid prawns. J. exp. Mar. Biof.

Estapa et al., 1987), the slope of haemolymph concen:ration against external medium concentration is much higher than reported for other penaeid species (Table 2). l’he decrease in respiration rate shown at low salinity (Fig. 3) is not shown by other species for which data exist. P. aztecus shows little change in respiration rate at salinities of 10, 20 and 3O’L (Biq;hop et al., 1980), whereas P. in&us shows a 300% increase in its respiration rate if the salinity is lou’ered from 37 to 10%0 (Dalla Via, 1986). These results suggest, respectively, osmoconforming and osrnoregulating organisms. ‘I’he results of the salinity tolerance experiments (Table 1) are supported to some extent by the work of 41-Abrani (1980), where a similar salinity range wasi demonstrated, although the animals survived for a much longer period. Farmer et al. (1979) showed that postlarvae of P. semisulcatus have an optimal salmity similar to that of the adults (i.e. 40X). In this respect P. semisulcatus is unusual, since its larvae do no-: have a brackish water phase, all evidence suggesting that they are found in inshore waters (Ai-Attar, 1979). From the results of my experiments, it seems that P. semisulcatus adults are also atypical in l-elation to other penaeid species in being the least euryhaline of the species for which there are published data.

Ecol. 54, 55+l.

Dal1 W. and Smith D. M. (1981) Ionic regulation of four species of penaeid prawn. J. exp. Mar. Biol. Ecol. 55, 219-232. Dalla Via G. J. (1986) Salinity responses of the juvenile shrimp Penaeus japonicus. 1: Oxygen consumption and estimations of productivity. Aquaculture 55, 297-306. Drobysheva S. S. and Aseev V. P. (1976) On the life cycle of Penaeus semisulcatus (Crustacea, Decapoda, Penaidae) in the Persian Gulf. Zoologichekij Zhurkal 5, 769-771. Farmer A. S. D. and Ukawa M. (1986) A orovisional atlas for the commercially important penaeid shrimps of the Arabian Gulf. Kuwait Bull. Mar. Sci. 7, 234. Farmer A. S. D., Watanabe T., Al-Ameeri A. A., Al-Hassan K. E., Al-Hajj A. B. and Salman S. E. (1979) Commercial culture of penaeid shrimps to marketable size. Kuwait Institute for Scientific Research, Annual Research Report, 5 l-52. Ferraris R. P., Parado-Estepa F. D., Ladja J. M. and de Jesus E. G. (1986) Effect of salinity on the osmotic, chloride, total protein and calcium concentrations in the haemolymph of the prawn Penaeus monodon (Fabricius). Comp. Biochem. Physiol. 83A, 701-708.

Harrison P. J., Waters D. E. and Taylor F. J. R. (1980) A broad-spectrum artificial seawater for coastal and open ocean plankton. J. Phycol. 16, 28-35. Lange R. (1972) Some recent work on osmotic, ionic and volume regulation in marine animals. In Oceanography and Marine Biology Annual Review (Edited by Barnes H.) Vol. 10, pp. 97-136. MacFarland W. N. and Lee B. D. (1963) Osmotic and ionic concentrations of penaeidean shrimps of the Texas coast. Bull. Mar. Sci. Gulf and Carribean 13, 391417.

Acl:nowledgemenfs-This work was carried out whilst in receipt of a Kuwait University research grant (SDZ 203). I wolld like to thank the Kuwait Institute for Scientific Research, and in particular Dr J. M. Bishop, for supplying livcmshrimps.

REFERENCES

Al. Abrani M. (1980) The effect of salinity on Penaeus :~emisulcatus. Report PP1013/FRM-RT-R-8002, Kuwait

Institute for Scientific Research. Al, Attar

M. H. (1979) Distribution and abundance of Penaeid larvae in Kuwait Bay and adjacent waters. .Kuwait Institute for Scientific Research, Annual Research Iceport, 46-47.

Mathews C. P., Samuel M. and Al-Attar M. H. (1979) The oceanography of Kuwait waters: some effects on fish populations and on the environment. Kuwait Institute for Scientific Research, Annual Research Report, 65-70. Panniker N. K. (1986) Osmotic behaviour of shrimps and prawns in relation to their biology and culture. Fishery report of the Food and Agriculture Organisatior, 57, 527-538. Parrado-Estepa F. D., Ferraris R. P., Ladja J. M. and de Jesus E. G. (1987) Responses of intermolt Penaeus indicus to large fluctuations in environmental salinity. Aquaculture 64, 175-184.

Williams A. B. (1960) The influence of temperature on osmotic regulation in two species of estuarine shrimps (Penaeus). Biol. Bull. Woods Hole 119, 56&571.