OXYGEN CONSUMPTION AND SALINITY TOLERANCE IN FOUR ...

OXYGEN

AND SALINITY CONSUMPTION IN FOUR BRAZILIAN CRABS

TOLERANCE

BY SANDRA E. SHUMWAY Department of Ecology and Evolution, State University of New York at Stony Brook, Stony Brook, New York, 11794, U.S.A. ABSTRACT and mean tolerance level at varying salinities were Oxygen consumption for four species of Brazilian crabs: Panopeus herbstii, Callinectes danae, determined inPetrolisthes armatus and Pachygrapsus transversus. The oxygen consumption creased and tolerance levels decreased in dilute seawater in all species. The tolerance level of each crab reflects its lifestyle and habitat. P. armatus, found salt water, had the lowest tolerance level to only in channels of free-moving dilute seawater and P. transversus, a shore crab, had the highest level of all the rate at all species studied. C. danae showed the highest oxygen consumption salinities. This is presumed to be a result of its more active nature. P. transversus in all salinities less than demonstrated the lowest rate of oxygen consumption 60% seawater. INTRODUCTION zone are frequently Marine animals occupying the intertidal subject to variations in the ambient salinity. While there have been numerous studies on in crustaceans the effect of salinity on tolerance and oxygen consumption (for review see Kinne, 1971), there have been few studies of this sort comparing are species from the same general area. Four species of decapod crustaceans Sdo Sebastiao, on the shore at the Marine found commonly Laboratory, to determine the effect of salinity on the Brazil, and a study was undertaken and the species' tolerance to seawater dilution. oxygen consumption MATERIALS AND METHODS Three species of brachyuran crabs, Panopeus herbstii H. Milne Edwards, 1934, Callinectes danae Smith, 1869, Pachygrapsus transversus (Gibbes, 1850) and Petrolisthes armatus (Gibbes, 1850) were collected at one species of Porcellanid, Brazil (23°49'44"S SAo Sebastido, Panopeus herbstii is a mud 45°25'27"W). crab found under rocks and in small tidepools and crevices, C. danae, a swim-

77 ming crab, is an entirely aquatic species, Petrolisthes armatus, a porcellanid crab, is found commonly under stones near free-flowing seawater and Pachygrapsus transversus is a species commonly found under rocks and crawling on the undersides of boulders and is normally exposed to full strength seawater; however, heavy rains often subject the crabs to dilution in tidepools. and salinity tolerance of these species were measured Oxygen consumption in 0, 20, 40, 60, 80 and 100°/0o seawater (100°/0o s.w. = 34°/00) at ambient Seawater dilutions were prepared temperature (25°C). by adding distilled water to local seawater. The dry weight for each specimen was determined by oven drying for 24 hours at 60 ° C . Ten crabs were placed in covered glass crystallizing dishes with equal volumes (3 litres) of each experimental Sexes were not separated. salinity. Since C. danae is much larger than the other species studied, five animals were placed in each of 2 dishes at each salinity. The water was aerated continuously and changed every 24 hours to prevent the build-up of toxic wastes. ExThe crabs were checked for survival periments were carried out in duplicate. and activity every 30 minutes for the first 8 hours, and then at 24 hour intervals for 5 days. The animals were not fed during the experiments. The activity of each crab was assessed using a system previously described by Preece (1970) and Jones (1976): freely moving and active, 2 points; lethargic and failure to 1 point; dead, 0 points. Thus a maximum move after gentle prodding, tolerance score (20) indicated that all 10 crabs in a given salinity were active indicated reduced tolerance and sugand healthy. Scores less than maximum gested that animals were under stress. The acute response of oxygen consumption to salinity change was measured salinities for 1 hour in all four species. Crabs were exposed to the experimental to measurement of was prior oxygen consumption. Oxygen consumption monitored a Radiometer electrode connected to a Beckman oxygen gas using analyser. RESULTS The mean tolerance scores for the four species of crabs exposed to 0, 20, 40 and 60% seawater are shown in fig. 1. There were no adverse effects on any species at 80 or 100% (control) seawater. The first indication that the tolerance occurred at 60% seawater for Petrolisthes armatus, 40 % level was diminished for Panopeus herbstii, 207o seawater for C. danae and only at 0 % seawater seawater for Pachygrapsus transversus. It appears then, that Petrolisthes armatus has the lowest tolerance of the four species to reduced salinity, although all four of the species studied showed some tolerance to seawater dilution. for the four species Fig. 2 shows the effect of salinity on oxygen consumption studied. C. danae and Pachygrapsus transversus showed the same general pattern for both species was in their response to salinity change. Oxygen consumption from 40-100% seawater; further dilution unaffected by salinity concentrations

78 rate. Maximum seawater yielded a gradual increase in metabolic rate was reached in 0 9lo seawater. Panopeus herbstii showed oxygen consumption in dilutions as low as 60 % seawater. It then no change in cxygen consumption from 40-0% seawater, in with a increase responded sharp oxygen consumption in Petrolisthes armatus showed a gradual inmaximum seawater. a 0% reaching crease in oxygen uptake from 100 to 60% seawater. Maximum oxygen conand then decreased occurred at 20% seawater rapidly in 0% sumption seawater. C. danae showed the highest overall rate of oxygen uptake rate of the four species in all salinities tested.

to 20%

Fig. 1. Mean tolerance scores for 4 species of crabs in 0, 20, 40 and 60% seawater. (Tolerance scored as 2 points for each active animal, 1 point for each lethargic animal and 0 for each dead animal). DISCUSSION rate increased in all four results reported here show that respiratory seen commonly in a dilute when to seawater, response exposed species Rao has that the rate of studies. oxygen suggested Pampath (1958) previous of many species of crustaceans depends on the salinity of the consumption medium to which the animals are naturally adapted. He showed that brackish of Metapenaeus monoceros (Fabricius, water specimens 1798) demonstrated minimum metabolic activity in 50 % seawater and that their rate of oxygen The

79 increased in both concentrated and dilute salinities. The oxygen consumption rate increased with increased differences in osmotic concentraconsumption tion between the blood of the prawn and the external medium. A similar has also been Flemister & Flemister who showed response reported by (1951) that the oxygen uptake of Ocypode quadrata (Fabricius, 1787) (as 0. albicans) was lowest when the crabs were isotonic with the external medium. Lofts (1956) found that the minimal rate of respiration for two populations of Palaemonetes varians (Leach, 1814), one a sluice pool species the other a marsh pool inhabitant, was seen when the animals were isotonic with the external medium. King

Fig. 2. Oxygen consumption in 4 species of crabs as a function of salinity. Error bars represent 95% confidence limits.

80 Carcinus mediterraneus Czerniavsky, 1884, (1965) studied two osmo-regulators, rate inand Callinectes sapidus Rathbun, 1896, and found that the respiratory creased in dilute seawater when compared with the rate in normal seawater. Dimock & Groves (1975) found that oxygen consumption for the mud crab as herbstii increased decreased and more Panopeus salinity recently Shumway & rate in the estuarine crab Jones (1981) have shown an increased respiratory Helice crassa Dana, 1852, when exposed to seawater concentrations differing from those to which it was adapted. The results from this experiment show the oxygen consumption response and tolerance level to varying salinities of four intertidal crabs to bear a direct to the individual relationship species' habitat. Petrolisthes armatus showed the lowest tolerance level of all four species. Petrolisthes elongatus (H. Milne Edwards, 1837), a related species, has been shown to be a stenohaline species crabs, Pisidia longicornis (Jones, 1976), although two other species of porcellanid (Linnaeus, 1767) and Porcellana platycheles (Pennant, 1777) can penetrate dilute seawater areas (Wolff & Sandee, 1971 ). Petrolisthes armatus in the present study are only found near areas of free flowing seawater even during periods of low tide, clearly avoiding dilute water in tide pools and it seems evident that salinithe local distribution of this species. ty is a major factor in determining to be of herbstii is known tolerant dilute seawater (Wells, Panopeus highly Dimock & and the 1961; Daves, 1974; Groves, 1975) present findings are in to note that of the four species with past studies. It is interesting agreement studied here, P. herbstii ranks third in its tolerance to fresh water exposure and that in the study area, despite its high tolerance of low salinity, it is normally found in high salinity areas. The swimming crab, Callinectes danae, showed no ill-effects until it was exincreased significantly posed to 20% seawater after which oxygen consumption and survival decreased. Other species of Callinectes have been shown to be highly tolerant of fresh water (Brues, 1927; Pearse, 1936) and its relatively high overall rate of oxygen consumption is apparently attributable to its active lifeGilles demonstrated an increase in the oxidative style (Ayers, 1938). (1973) in metabolism of amino acids isolated axons of C. sapidus following acclimation in oxydative to reduced His data indicate that modification salinity. metabolism observed during osmotic stress can be related to the variation in many euryhaline animals. The absence of observed in oxygen consumption indicates either that energy a marked effect of salinity on oxygen consumption for work are not met aerobic means or that, assuming osmotic requirements by in a high efficiency, the increment required for osmotic oxygen consumption work is too small to be detected (Potts & Parry, 1964). level of all species, Pachygrapsus transversus showed the greatest tolerance of stress in its first seawater. 0% demonstrating signs Oxygen uptake in this the same as the tolerance level, gradually increasing species following pattern in the lower salinities. P. crassipes Randall, 1840, close relative of P. transversus,

81 has been shown by Gross (1957) to be a good osmotic regulator in both hypoand hyper-osmotic media. P. transversus, unlike P. crassipes, did not show any increased activity associated with an escape response when exposed to dilute seawater. Gross suggested in his study that the increase in oxygen uptake in dilute seawater was a result of increased locomotor activity. Several theories have been formulated to explain this increase in respiration in low salinities. Gross (1957) suggested that behavioral avoidance responses to lowered salinity might contribute to the enhanced metabolic rate. Schlieper that in salt carbon concentrations, higher dioxide, a general (1971) suggested stimulant for cellular respiration, would be readily removed from the animal. In low salinities, however, there would be a tendency for carbon dioxide to acthus increasing respiratory rate. Lange et al. (1972) proposed that cumulate, the increased at lower salinity, coupled with oxygen-dependent solubility is responsible for enhanced oxygen consumption at reduced salinirespiration, The most is that the increased metabolic rate is ty. commonly proposed theory caused by increased osmotic work (Flemister & Flemister, 1951; Hagerman, however (Potts & Parry, 1970; Schlieper, 1964; 1971). There is evidence, that the metabolic demands of ion are not sufficient to King, 1965) transport the increased rates which occur in explain respiration many species exposed to dilute seawater. The results of the present study show Petrolisthes armatus to be the most stenohaline crab and Pachygrapsus transversus to be the most euryhaline with herbstii and danae to C. Panopeus being euryhaline varying degrees. ACKNOWLEDGEMENTS This

work would not have been possible without the use of facilities and hospitality extended to me by Dr. Joao Lunetta. I would also like to thank Drs. Gloria S. Moreira and Jorge Peterson for the use of equipment and helpful discussions. RÉSUMÉ La consommation d'oxygène et le niveau moyen de tolérance à différentes salinités a été déterminée pour quatre espèces de crustacés décapodes du Brésil: Panopeusherbstii, Callinectesdanae, Petrolisthesarmatuset Pachygrapsustransversus.Chez toutes les espèces, la consommation d'oxygène s'est accrue et les niveaux de tolérance ont décru dans l'eau du mer diluée. Le niveau de tolérance de chaque espèce reflète son mode de vie et son habitat. Petrolisthesarmatus, trouvé seulement dans les chenaux d'eau salée libre, avait le niveau de tolérance le plus bas et Pachygrapsus transversus,un crabe côtier, le niveau le plus élevé parmi les espèces étudiées, à l'égard de l'eau de mer diluée. Callinectesdanae présentait le taux de consommation d'oxygène le plus élevé à toutes les salinités. Ceci peut être considéré comme une conséquence de sa nature plus active. Pachygrapsus transversusa manifesté le taux de consommation d'oxygène le plus bas. REFERENCES AYERS, JohnC., 1938. Relationship of habitat to oxygen consumption by certain estuarine crabs. Ecology, 19: 523-527.

82 BRUES,C. T., 1927. The occurrence of the marine crab, Callinectes ornatus, in brackish and fresh water. Amer. Natural., 61: 566-569. DAVES,E. T., unpublished. Osmotic and ionic regulation in the estuarine mud crab Panopeus herbstii. Master of Science Thesis, 1974, Wake Forest University, 42 pp. DIMOCK,R. V. & K. H. GROVES,1975. Interaction of temperature and salinity on oxygen consumption of the estuarine crab Panopeus herbstii. Mar. Biol., 33: 301-308. L. J. & S. C. FLEMISTER, 1951. Chloride ion regulation and oxygen consumption in FLEMISTER, the crab Ocypoda albicans. Biol. Bull. Woods Hole, 101: 259-273. GILLES, R., 1973. Oxygen consumption as related to the amino acid metabolism during osmoregulation in the blue crab Callinectes sapidus. Netherlands Journ. Sea Res., 7: 280-289. GROSS,W. J., 1951. An analysis of response to osmotic stress in selected decapod Crustacea. Biol. Bull. Woods Hole, 112: 43-62. HAGERMAN, L., 1970. The oxygen consumption of Crangon vulgaris in relation to salinity. Ophelia, 7: 283-292. JONES, M. B., 1976. Limiting factors in the distribution of intertidal crabs (Crustacea: Decapoda) in the Avon-Heathcote Estuary, Christchurch. New Zealand Journ. mar. Freshwater Research, 10: 577-587. KING, E. N., 1965. The oxygen consumption of intact crabs and excised gills as a function of decreased salinity. Comp. Biochem. Physiol., 15: 93-102. KINNE, O., 1971. Salinity: Animals - invertebrates. In: O. KINNE(ed.), Marine Ecology, 1: 821-1083. (Wiley Interscience, London). H. & A. MOSTAD,1972. The effect of salinity and temperature on LANGE,R., STAALAND, solubility of oxygen and respiratory rate in oxygen-dependent marine invertebrates. Journ. exp. mar. Biol. Ecol., 9: 217-229. LOFTS,B., 1956. The effects of salinity changes on the respiratory rate of the prawn Palaemonetes varians (Leach). Journ. exp. Biol., 33: 730-736. PAMPAPATHI RAO, K., 1958. Oxygen consumption as a function of size and salinity in Metapenaeus monoceros (Fab.) from marine and brackish water environments. Journ. exp. Biol., 35: 307-313. PEARSE,A. S., 1929. Ecology of estuarine crabs at Beaufort, N.C. Journ. Elisha Mitchell sci. Soc., 44: 230-237. POTTS,W. T. W. & G. PARRY,1964. Osmotic and ionic regulation in animals: 1-423. (Pergamon Press, Oxford). PREECE,G. S., 1970. Salinity and survival in Bathyporeia pilosa Lindstrom and B. pelagica (Bate). Journ. exp. mar. Biol. Ecol., 5: 234-245. SCHLIEPER,C., 1971. Physiology of brackish water. In: A. REMANE& C. SCHLIEPER (eds), Biology of brackish water, (ed. 2): 211-350. (Wiley Interscience, New York). S. E. & M. B. JONES,1981. Influence of salinity on the respiration of an estuarine SHUMWAY, mud crab, Helice crassa (Grapsidae). Comp. Biochem. Physiol., 70 (A): 551-553. WELLS,H. W., 1961. The fauna of oyster beds, with special reference to the salinity factor. Ecol. Monogr., 31: 239-266. WOLFF,W. J. & A. J. J. SANDEE,1971. Distribution and ecology of the Decapoda Reptantia of the estuarine area of the rivers Rhine, Meuse and Scheldt. Netherlands Journ. Sea Res., 5: 197-226.