Salinity responses in brackish water populations of the freshwater shrimp Palaemonetes antennarius—I. Oxygen consumption

Camp. Biochem. Physiol. Vol. 87A, Printedin Great Britain

No. 2, pp. 471478,

1987

0300-9629/87 $3.00 + 0.00

0 1987 PergamonJournalsLtd

SALINITY RESPONSES IN BRACKISH WATER POPULATIONS OF THE FRESHWATER SHRIMP PALAEMONETES ANTENNARIUS-I. OXYGEN CONSUMPTION GIUSEPPEJOSEF DALLA VIA Abteilung Zoophysiologie, Institut fiir Zoologie der UniversitIt Innsbruck, Technikerstrasse 25, A-6020 Innsbruck, Austria. Telephone: (05222) 748-5306 (Received 22 August 1986)

Abstract-l. Rapid increases in salinity result in a mean increase in oxygen consumption of 54% which returns again to the initial level after 8-10 hr. Decreases in salinity produce an increase in the metabolic rate of only 20% which returns to the initial level again after 4-8 hr. 2. In steady-state experiments, the shrimps display the lowest oxygen consumption rates at low salinities. The lowest metabolic rates occur at a salinity of 2% and 5%. At 20% the shrimps exhibit up to 30% higher metabolism. 3. A comparison of three brackish water populations shows that the metabolic response to an acute change of salinity depends on the salinity to which the animals had been acclimated before. 4. On the basis of measured metabolic rates productivity estimations were undertaken and discussed in connection with earlier ecological findings. In 19% brackish water Paluemonetes untennarius lives at its physiological limit. There it does not grow, loses biomass, and probably only enters this area from authmn to spring.

INTRODUCTION Palaemonetes antennarius is a freshwater shrimp from the Mediterranean area that can be found mostly in lakes and rivers (Froglia, 1978; Dalla Via, 1985a). Although considered to he an oligostenohaline shrimp (Parry, 1957, 1961; Parry and Potts, 1965; Kinne, 1971; Knowlton and Kirby, 1984), in brackish

water it can populate the ecological niche where frequent and rapid changes in salinity occur (Dalla Via, 1983a). The effect of salinity on the oxygen consumption of crustaceans has already been discussed in many related reports (Dimcock and Groves, 1975; Gaudy and Sloane, 1981; Moreira et al., 1982, 1983; Nelson et al., 1977; Shumway, 1978; Simmons and Knight, 1975; Stephenson and Knight, 1981, 1982; Vernberg, 1983). The significance of oxygen consumption measurements lies in estimating the adaptive capacity of the organism. The changes in the metabolic rate following a change in salinity express the sum of metabolic processes and simultaneous behaviour changes rather than the energy expenditure of pure osmotic work (Kinne, 1971; Vernberg, 1983). Theoretical and thermodynamic considerations show that the energy expenditure of purely osmoregulatory work makes up only a few percent of the basic metabolism (Potts, 1954; Shaw, 1959; Potts and Parry, 1964; Styczynska-Jurewicz, 1970; Fletcher, 1976). This is also confirmed by experimental results (Bielawski, 1971; Sutcliffe and Carrick, 1975). In the border areas between fresh and brackish water, an organism is exposed to fluctuating salinities resulting from tides, rainfall and changing wind conditions several times a day (Findley et al., 1978; Dalla Via, 1983a). This is the case for Palaemonetes antennarius,

whose occurrence and ecology in fresh-water (Hofer et al., 1980) and brackish water (Dalla Via, 1983a) was studied. The goal of this investigation is to study oxygen consumption as a response to a change in salinity and to clarify the adaptation of this species to its ecological conditions. MATERIALS AND Specimens

The animals originated from the Lagoon of Lesina, a brackish water lagoon in southern Italy (Marolla, 1980; De Angelis, 1953, 1963; Dalla Via, 1985a). The shrimps used for respirometry were caught at three different locations in and around the lagoon: (1) San Nazario. A warm spring with a temperature of 27-28°C and a low salinity of 2%. (2) Idrovora De Pilla. A drainage system with pumping station for drainage of fields with a mean salinity of S-8%. (3) East of the Canale Lauro inflow with a salinity of 19%. More detailed information regarding the capture locations, the population structure and their ecology can be found in an earlier report (Dalla Via, 1983a). The shrimps were acclimated for at least 24 hr in the original water, maintained at 20°C and not fed. As the environmental water temperature at the time of the experiments was around 20°C and the oxygen consumption measurements were carried out at 2o”C, a longer temperature adaption was not necessary. The experimental salinities were established by distilled water and artificial sea-water salt. The required salinity was controlled with a hand refractormeter (American Optical Corp.). Respirometry The oxygen measurements were carried out with two intermittent-flow respirometers according to Forstner

471 c BP 870--0

METHODS

412

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JOSEF

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Temperature

contra

-

Fig. 1. The intermittent-flow respirometer used for the oxygen consumption measurements. SM = stirring motor; HC = heating and cooling unit; heating coils; stirring unit to roll round the water from the water bath. and by magnetic coupling to pump the medium in the animal chambers. V = sequencing valve; VM = valve motor; T = thermistor; RB = reserve medium bottle; C = connecting unit.

(1983a,b) and Dalla Via (1985b) (Fig. 1). Each respirometer is a four-cham~r-system in which each animal chamber, in succession, is automatically locked into a closed measurement cycle by way of a sequencing valve. The oxygen consumption of the shrimps in the animal chamber was recorded as the decrease of dissolved oxygen in the water (starting with a 100% air-saturated medium) by means of a polarographic oxygen sensor. During the measurement procedure in one animal chamber, Aow through is maintained in the other three chambers, which are supplied with air-saturated medium from a storage bottle. The oxygen consumed by the bacteria during the experiment were taken into account and subtracted from the metabolic rate of the shrimps (Dalla Via, 1983b). The relatively small biomass of the shrimps compared to the dead volume of the measurement system made it necessary to place several animals in each chamber. In order to avoid crowding, the eight shrimps per animal chamber were separated from each other by steel net cages (Dalla Via, 1986). The cages were made of stainless steel nets (mesh width 2.5 mm) with four compartments on top and four at the bottom, where one shrimp was confined to each compartment. Since the cages were relatively small, the shrimps showed no more than a “crawling activity” and no swimming activity. Since there are eight shrimps per animal chamber in the respirometer, each

respirometer measurement value is an average of the oxygen consumption of these eight shrimps. Care was always taken that shrimps of the same size class were placed in one animal chamber. Intermoult animals were used for the oxygen consumption measurements. However, if a stress-induced moult did take place in the respirometer the experiment was rejected. Table 1.

~_.._ $ Pov P egg

RESULTS Oxygen consumption

of P~iuemonetes ante~narius

at the respective environmental salinity is presented in Table 1. From this it appears that higher oxygen consumption is found in specimens from areas of higher salinity. Males as well as females with eggs in the ovary in the 2%0 and 6%0 populations show similar oxygen consumption values. In the 19L population, the oxygen consumption rates he higher for males. The fluctuating salinity stress of various brackish water populations of Palaemonetes antennarius can be seen in Figs 2-5. Generally it can be observed that a sudden rise in salinity brings a high increase in oxygen consumption. A salinity decrease causes only a slight increase in the metabolic rate. Figure 2 shows the oxygen consumption of the population from San Nazario, which at 2%0, comes closest to a fresh-water population. A high increase in the oxygen consumption with an increase in salinity is visible. No effect on the oxygen consumption rate is evident by lowering the salinity to the original level. Figure 3 shows the oxygen consumption of the population from Idrovora De Pilla, which occurs primarily in 6%0 brackish water. When salinity is raised, a high increase in oxygen consumption is evident. However, the return to lower salinity also produces a small increase in the metabolic rate. In the brackish water population of Lauro, which has been

Steady state oxygen consumption of three different brackish water populations from the Lagoon of Lesina 6% 19% 2% (Idrovora) (San Nazario) (Laura) ______---.-.-_ --. -pti pmol 0,/g per hr MIN Par pmol 0,/g per hr M,N Par pmol 0,/g per hr M/N

9.064 + 0.623 12/l 9.070* 1.137 2512 6516~0.199 201I

10.362 j; 0.644 18/2 8.916 + 0.404 l2ll 6.654 I 0.351 14/i

12.215 It 0.782 2812 9.605 + 0.804 2812 -

The shrimps are field-adapted to temperatures of around 20°C. Measurement of the oxygen consumption took place at 2OC and the given field salinity. Oxygen consumption is given in pmol 0,/g per hr for males (d), females with eggs in the ovary (P ov), and females with eggs on the pleopods @egg). M = number of hourly measurement values from N long-term experiments.

473

Salinity responses in Palaemonetes antennarius 40

Palaemonetes Lagoon

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5 20

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0

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20 t;me

30

40

50

in hours

Time course of the oxygen consumption of a brackish water population of Palaemonetes from San Nazario (a 2% field adapted shrimp population) with repeated salinity shocks indicated by arrows. Weight classes (mg): (8 87 + I3), ---(0 233 + 30), --(0 239 & 34), -.(9 337 & 45). Fig.

2.

antennarius

oxygen consumption meaurements in Pulaemonetes antennarius from the Idrovora De Pilla population (6%0) acclimated to a salinity of 30% over a 3-day period. In comparison to Fig. 3 it is evident that high salinity adaptation leads to a more pronounced

adapted to 19%, the return to lower salinity also leads to a high increase in the metabolic rate (Fig. 5). Contrary to the other populations, this increase in the metabolic rate is maintained for many hours and no longer returns to the initial level. Figure 4 shows

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ontennarius Lesfna

it

0

10

30

20 time

in

40

50

60

hours

Fig. 3. Time course of oxygen consumption of a brackish water population of Palaemonetes antennarius from Idrovora De Pilla (a 6-8960 field adapted shrimp population) with repeated salinity changes (arrows). Weight classes (mg): (8 179 k 60), ----(6 245 _+ 63), ---(Oov 473 + 60), -.-.(9 egg 535 k 61).

GIUSEPPEJOSEFDALLAVIA

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Leslna

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30-L. I

0

I

10

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20

I

Time

in

I

40

30

50

60

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Fig. 4. Time course of oxygen consumption of a brackish water population of Paluemonetes antennarius from Idrovora de Pilla (6-t% adapted), which was acclimated to a salinity of 3Os60for a 3-day period before the start of the experiment. The sharp changes in salinity are marked by arrows. This form, acclimated to 300/msalinity, shows a more pronounced metabolic response to lowering the salinity than the mother population in Fig. 3. Weight classes (mg): ---(0 ov 386 + 121),(0 ov 511 + 76), -‘-

(0 egg 643 + 72). metabolic response to lowered salinity in this shrimp (Fig. 4). The adaptation salinity influences the amplitude of the metabolic response. After an acute salinity change

Polaemonetes Lagoon

0

10

of

20

from a low to a high salinity, the increase in metabolic rate declines with increasing adaptation salinity and vice versa (Fig. 6). Thus, after an acute change from a high to a low salinity, the metabolic response

antennarus Leslna

n

30 time

40

50

60

70

in hours

Fig. 5. Time course of the oxygen consumption of Palaemonetes antennarius from Lauro (a 10% field adapted shrimp population) and the metabolic response to fluctuating salinity. The sharp changes in salinity are designated by arrows. Weight classes (mg): (d 146 f 20), ---(6 152 + 34), --(dov 308 k 42), --(6 ov 351 + 83).

Salinity responses in Palaemonetesantennarius salinity increase from 2-7s to 30-32%

475

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Fig. 6. Maximum increase in the oxygen consumption (in %) of the three different brackish water populations of Palaemonetesantennariusafter salinity shocks in relation to adaptation salinity. The increase in oxygen consumption was calculated as the difference between the oxygen consumption before the salinity shock (initial condition 100%) and the highest metabolic rate after the salinity change. The corresponding population and adaptation salinity, the metabolic increase of single salinity change experiments (circles), their mean value (triangles), and the standard deviation (shaded area) are given in the diagram. The mean values were connected by a straight line. Population X is made up of shrimps from Idrovora De Pilla (&80/Wsalinity field adapted shrimps), which were acclimated to 30% sea-water for 3 days. The mean value of the population was entered on the connecting line Idrovora-Lauro. Condition A for the Lauro population presents the metabolic increase starting from the heightened metabolic level at 5%~ (see also Fig. 5). Condition B presents the metabolic increase starting from the recovered oxygen consumption level, comparable to the time course characteristics of population X. The freshwater population from Lake Garda was adapted for more than 3 weeks at 3%.

increases with increasing adaptation salinity. Here it is important to observe that a 3-day acclimation to a salinity of 30% is sufficient to cause a shift in the salinity response (Fig. 6, population X). Figure 7 shows general features of the salinity response. After an acute change from 2-W& to 30-32% oxygen consumption of Palaemonetes antennarius increases by 54% and approaches the initial value again after 8-10 hr (Fig. 7a), whereas by lowering the salinity from 30-32% to 2-W& oxygen consumption in-

creases by only 20% and recovery takes place after 48 hr (Fig. 7b). DISCUSSION Salinity response Palaemonetes antennarius is a fresh-water species which can also populate ecological niches in brackish water areas up to a salinity of 20%0 (Dalla Via, 1983a). P. antennarius can temporarily adapt well and relatively fast to changed salinity conditions. After a sudden change in salinity, the shrimp adjusts its metabolism back to the initial level within 8-10 hr (Fig. 7). This is a sign of a high capacity for compensatory adjustment in short-term adaptation. In longterm adaptation however, Palaemonetes antennarius

exhibits an increased oxygen consumption at 19% (Table 1). At this salinity the shrimp shows an up to 30% higher routine metabolism, this also in freshwater populations (Dalla Via, in preparation). The brackish water population exhibits a relatively wide range of resistance up to a salinity of 25% after 48 hr (Dalla Via, 1983a). Increased energy metabolism and mortality at higher salinities indicate that Palaemonetes antennarius populates the ecological niche of frequent and periodical salinity fluctuations, but cannot migrate into salinities above 20% for longer periods of time (see also Dalla Via, 1983a). Low salinity adapted shrimps (San Nazario, 2%) show the highest metabolic increase as a result of a salinity shock from 2% to 30°+ and practically no response to a decrease in salinity from 30% to 2% (Fig. 2). The metabolic response of Palaemonetes antennarius caused by a sudden change in salinity, changes with increasing adaptation salinity (Fig. 6). At higher adaptation salinities (Idrovora De Pilla 6-8%0, Lauro 19960),the metabolic increase due to the increase in salinity (from 2-8s to 30-32s) lessens. On the other hand, metabolic response increases following a sudden decrease in salinity from 30-32s to 2-8omO.In the 19% field adapted shrimps, a sharp decrease in salinity causes an increase in oxygen

416

GIUSEPPEJOSEF DALLA VIA

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-2

0

2 time

6

4 in

e

10

12

14

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Fig. 7. General average response of oxygen consumption salinity

to a sharp change in salinity (a) an increase in from 2-89/w to 3%32’S+ (b) a decrease in salinity from 3632t to 2-8L. N-number of averaged experiments; the standard deviation is represented by the shaded area.

consumption which stabilizes to a new metabolic level (Fig. 5). After a 3-day acclimation to 30%0, shrimps from the 60/w field-adapted population (Idrovora De Pilla) show a higher and much more distinct metabolic response to lowering the salinity than the original population (Figs 3 and 4). Thus in their response the shrimps clearly begin to shift near the values of 19% adapted animals and this happens after only a 3-day acclimation (Fig. 6). The Palaemonetes antennarius adapted to 19%0 (Lauro) are certainly living at their tolerance limit (Dalla Via, 1983a) and only migrate into these ranges of salinity. The salinity tolerance range of this population of Palaemonetes anfennarius (from 5%0to 30%0) shifted towards higher salinities, and the mortality increases below a salinity of 5% (Dalla Via, 1983a). On the other hand, the heightened level of oxygen consumption after a salinity reduction could express that the animals adapted to 19% have problems being exposed again to low salinities or to freshwater. Similar population differences are also found by Lofts (1956) in Palaemonetes varians, the nearest relative of P. antennarius. Comparing a low salinity (annual average 1.3%0) with a high salinity (annual average 23.5%0) adapted population, he has found that both respire least at the salinity of the environment they came from. At lower, as at higher salinities, the metabolic rate increases (Lofts, 1956). In general, oxygen consumption of P. antennarius increases by an average of 54% after a sharp increase in salinity and only by 20% after a sharp decrease in salinity (Fig. 7). This response differs from that of euryhaline gammarid species which after an acute salinity change from 10 to 300%0show no change in oxygen consumption or only variations of 10% around the

normal value. After a reversed change of salinity from 30 to l0%0, the oxygen consumption of the gammarids exhibits a high increase up to 70% of the initial value (Bulnheim, 1972). Also the moderate euryhaline hermit crab Pagurus bernhardus with shells shows a 45% increase in oxygen consumption after a sharp decline in salinity and no increase after a sharp rise in salinity (Shumway, 1978). Productivity Palaemonetes antennarius needs more energy in an environment of changing salinity, regardless of whether the salinity-induced high oxygen consumption is attributed to purely metabolic processes or to behaviour changes. This energy can be gained by higher assimilation or/and reduced production. In fact in the field one finds a reduced body size and weight of Palaemonetes antennarius from station Lauro with a salinity of 19X (Dalla Via, 1983a). This shrimp exhibits a lower energy content in the whole animal (17.4 + 0.9 kJ/g dry wt in males, N = 16) in comparision to the 5X field-adapted shrimps from the Idrovora De Pilla station (19.3 k 0.9 kJ/g dry wt in males, N = 5) (G. J. Dalla Via, unpublished). The high protein content of 48.8% (at 19% salinity) in comparison to 42.4% (at 5X salinity) also indicates that the percentage of carbohydrates and lipids at 190/w has dropped accordingly. From this ensued that the shrimps in high salinities possess less stored energy. Only 2-year-old males migrate into high salinity water. Comparing the ecological data of these specimens from station Idrovora (So/,) with those from the station Lauro (19%) we found a mean fresh weight of 257 mg for the former and 110 mg for the latter

417

Salinity responses in Palaemoneles antennarius Table 2. Mean fresh body weight of I- and 2-year-old males at different salinities in the Lagoon of Lesina (details in Dalla Via, 1983a) Environmental salinity

I -year-old males

2-year-old males

5+5% (Idrovora d.P.) 8% 14% l9?& (Laura)

122mg

257 mg

99 mg 72 mg

207 mg 122mg IlOmg

Acknowledgements-This

research was supported by the Fonds zur Foerderung der wissenschaftlichen Forschung in

C)sterreich, project no. 3307 and by the Oesterreichische Nationalbank, project no. 1208. I thank Prof. W. Wieser for critically reviewing the manuscript and Prof. F. Lumare for his kind hospitality at the Laboratory for the Biological Exploitation of the Lagoons, Lesina, Italy. REFERENCES

J. (1971) Energetics of ion transport in the gill of the crayfish Astacus leptodactylus Esch. Comp. Biochem.

Bielawski

Physiol. 39B, 649-657.

specimens (Table 2, Dalla Via, 1983a). The yearly biomass production between l-year and 2-year-old male Palaemonetes antennarius in Lake Garda is 18.8 g/m* at a population density of 772 shrimps/m* (Hofer et al., 1980) of which 25% are males (Dalla Via, 1983a). We obtain from this data a yearly production of 97 mg for an l-year-old male shrimp in In comparison, assuming that Lake Garda. l-year-old males from 5% adapted salinity from the Lagoon of Lesina migrate to the 19%0 region of Lauro, we find no growth occurring between l-year-old (at So/,) and 2-year-old males (at 19%0). Both show the same size (Table 2, and length distribution in Dalla Via, 1983a). Palaemonetes antennarius from the Lauro station (19% salinity) has a higher metabolic rate (increased by 1.9 pmol 0,/g per hr, Table 1) at 20°C than Palaemonetes antennarius from the Idrovora De Pilla station (5%). Considering this metabolic increase and correcting it with respect to the average monthly temperature in the Lagoon of Lesina over the period of one year as reported in Dalla Via (1985a, from Marolla, 1980; Q,,-values from Dalla Via, in preparation), we find that a 250 mg shrimp (2-year-old male) consumes 2.96 mmol O,/year more in 19% salinity than in 6%0 adapted animals. Assuming 30% protein, 30% lipids, and 40% carbohydrates as catabolized respiratory substrates, we can estimate (according to Gnaiger, 1983) the biomass loss due to this higher metabolism to be 250 mg/year. If this shrimp only lives in a 19% salinity from September to April, it then loses 115 mg of ash-free organic biomass. This is approximately as much as the production amounts to in freshwater (see above). A 2-year-old male shrimp (257 mg) therefore loses so much organic biomass that it remains at the weight of a l-year-old (for ecological data see Dalla Via, 1983a). The loss may even be higher under the influence of fluctuating salinities as they occur in the environment. This theoretically estimated loss of biomass makes it clear that in 19%0 brackish water Palaemonetes antennarius lives at its physiological limit. It does not grow, loses biomass, and probably only enters these areas temporarily during winter months. This aspect would also explain why females make up not more than 25% of the population in 19%, and of these only 3.7% carry eggs on their pleopods during the main reproduction period (Dalla Via, 1983a): They do not have the energy for egg production, which amounts to about 10% of total body weight. It can be summarized that high salinity conditions and frequent salinity changes are energetically incompatible with growth and reproduction for Palaemonetes antennarius in this environment.

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