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Seasonal migration of the swimming crab macropipus holsatus in an estuarine area controlled by tidal streams
Netherlands 3ournal of Sea Research 7 : 94-102 (1973) 7th European Symposium on Marine Biology
SEASONAL MIGRATION OF THE SWIMMING CRAB MACROPIPUS HOLSATUS IN AN ESTUARINE AREA CONTROLLED BY T I D A L STREAMS by S. C. VENEMA* and F. CREUTZBERG (Netherlands Institutefor Sea Research, Texel, The Netherlands)
CONTENTS I. II. III. IV. V. VI. VII.
Introduction . . . . . . . . . . . . . . . . . . . . Hydrography of the Dutch Wadden Sea . . . . . . . . . . . . . . Fishery surveys. . . . . . . . . . . . . . . . . . . Mechanism of migration . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . Summary . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
94 95 95 97 99 101 102
I. I N T R O D U C T I O N The swimming crab Macropipus holsatus (Fabricius) is a common inhabitant of the open North Sea the whole year through, but in spring the animal extends its geographic distribution into estuarine areas, withdrawing again in late autumn. These movements have been reported by VERWEY (1958) for the Dutch Wadden Sea and by WOLFF & SANDEE (1971) for the estuarine area of the rivers Rhine, Meuse and Scheldt. In the present paper, the results of a study of these seasonal migrations, carried out during fishery surveys in the Dutch Wadden Sea in the years 1961 through 1964 in cooperation with our colleague M. Fonds will be given, as well as the results of laboratory experiments --carried out in 1962--on the possible mechanism underlying these migratory movements. Acknowledgement.--The authors wish to express their gratitude to Mr J. A. A. Spiekerman (The Hague) for correcting the English text. * Present address: Fisheries Resources Devision, Research Information Section, FAO, Roma, Italy.
MIGRATION
OF SWIMMING
CRABS
95
II. HYDROGRAPHY OF THE DUTCH WADDEN SEA The geomorphological structure of the Dutch Wadden Sea demonstrates the dominant role played by the tidal currents. According to POSTMA (1954) the distances covered by floats during a complete flood tide or ebb tide range between 10 and 24 km depending on the size of the tidal channels. Formerly the Wadden Sea and the Zuiderzee formed one open system. By the construction of the Afsluitdijk in 1931 the brackish Zuiderzee was gradually turned into a fresh water lake, the IJsselmeer. The salinity of the Wadden Sea, therefore, is mainly determined by the amount of fresh water discharged (at low tide) at the 2 sets of sluices located at both ends of the Afsluitdijk, with the result that the Wadden Sea is characterized by a salinity gradient ranging from about 18 ~oo near the A/'sluitdijk to approximately 30 ~o S in the tidal inlets between the islands (Fig. lf). In dry periods, when discharges of fresh water are stopped for some months, virtual marine conditions may occur in the Wadden Sea. Salinities vary greatly, with extreme differences being found near the Afsluitdijk. These variations are caused both by variations in the amounts of fresh water discharged by the sluices, and by tidal movements shifting the whole salinity gradient up and down. As for temperature, roughly similar types of gradients are observed in autumn, as a result of more rapid cooling of the shallow inland water than of the North Sea water in a period of decreasing air temperature. In spring, however, the salinity and temperature gradients show exactly the reverse picture, as a result of more rapid warming of the inland waters (PoSTMA, 1954). III. FISHERY SURVEYS In this area, monthly fishery surveys were carried out from October 1961 to October 1962 and from September 1963 to October 1964, using a 2½ metre beamtrawl and a I0 metre ottertrawl, respectively. All the catches were converted into numbers of animals per 1000 m 2. The distribution of swimming crabs appeared to be fairly regular through certain periods. This enabled us to average the catches made during selected groups of succesive months. The mean density of Macropipus holsatus in September, October and November 1963 at the different stations reveals that the swimming crabs show a preference for the outer area of the Wadden Sea and tend to avoid the brackish areas along the Afsluitdijk and the Friesland coast (Fig. la). The assumption that the furthest extent of penetration into a brackish area is determined by the decreasing salinity is also suggested by POULSEN (1922, 1949) for swimming crabs in the Kattegat area, where they are
96
S. C. V E N E M A
& F. C R E U T Z B E R G
not found in water of a salinity below 20 to 23 %0 S. WOLFF & SANDEE (1971) suggest a salinity not far below 27 %o as the limit of occurrence in the Rhine, Meuse and Scheldt estuary. There are indications that the salinity-dependent limit of occurrence in turn is influenced by temperature. In the winter months (December 1963 to March 1964) the crabs were found entirely or almost entirely withdrawn from the Wadden Sea (Fig. lb). Similar observations had been made in the winter of 1961 tot 1962. meon densily per I 0 0 0 rn= 0
I
•
2I0 II- 50 51- ;00 I01 - 2 0 0 201 - 4 0 0
•
4ol - 8oo
-,-,-
,o"1
,.
t~' e
Fig. 1. a-e. Distribution of Macropipuaholsatus in the western W a d d e n Sea expressed as numbers caught per 1000 m a over different seasons, f. Distribution of average surface salinity in 1962 in the western W a d d e n Sea.
M I G R A T I O N OF S W I M M I N G C R A B
97
Starting in April 1964, a gradual resettlement in the Wadden Sea took place, while again the extent of penetration appeared to be restricted to the more saline outer parts of the Wadden Sea during spring and early summer until June (Fig. lc). In August and September 1964, however, a remarkable extension of their distribution to the Afsluitdijk and the Friesland coast was observed (Fig. ld). Unfortunately our hydrographical data do not permit definite conclusions, but it is a fact that just prior to this time the fresh water discharges at the Afsluitdijk had been considerably reduced for some months. In October 1964 the more normal distribution was found again; discharges of the normal volume of IJsselmeer water had been resumed some time previously. Another slight indication of a salinity-temperature controlled migration is found in the distribution of swimming crabs in March and April 1962, during surveys which additionally covered a more eastern as well as more saline part of the Wadden Sea. While in the western (more brackish) part no swimming crabs were observed yet, immigration was already taking place in the eastern area (Fig. le). IV. M E C H A N I S M
OF MIGRATION
An incidental observation in September 1945 of large numbers of Macropipus holsatus swimming in the surface water during the ebb where few or none had been seen during the flood tide (VERwEY, 1958), gave rise to the assumption that the crabs use the tidal currents as a means of transportation in their seaward migration in autumn and supposedly also for inward migration in the spring. Since the swimming power of M. holsatus is negligible in comparison to the velocity of the tidal currents, swimming seems to have significance only in keeping the animal suspended in the water layers and probably the crab may well have no other means of migration than that of passive transportation. In the autumn of 1965 a series of attempts were made, using a pelagic trawl, to establish a seaward pelagic transportation of swimming crabs. In most cases, however, no pelagically-swimming crabs were caught, and when they were, the numbers were too small and too variable to demonstrate any differences between ebb and flood catches. These few results do not permit conclusions. The experimental approach to the problem was based on the supposition that during ebb tide a decrease of salinity acts as releasing factor for swimming behaviour. In the laboratory, therefore, the animals were subjected to conditions simulating ebb and flood tide by changes of salinity under constant current conditions. The apparatus used was a modification of the circular tidal stream apparatus (outer diameter 80 cm) designed for migration studies of young eels (CREuTZ-
98
S. C. V E N E M A
& F. C R E U T Z B E R G
BERO, 1961). In the modified arrangement the water-current-generating paddies are placed in the inner cylinder to avoid disturbances by moving objects in the experimental channel (Fig. 2). The circular current is admitted into the experimental channel through horizontal inflow r
~ J ~ _ _ ~ overflow
~
outer cylinder inner cylinder paddles
Fig.2. Circular tidal stream apparatus. open slits in the wall of the inner cylinder. An inflow in the inner cylinder and an over-flow in the outer cylinder maintain constant water renewal in the whole system. By changing the quality of the supplied water any characteristic of the water in the experimental channel, such as salinity and temperature, can be gradually changed to any extent. In each experiment usually 10 swimming crabs were placed in the experimental channel where they were allowed to burrow in the sandy substrate. Each experiment was introduced by a period of constant salinity and temperature for 15 to 60 minutes. Next an ebb tide was simulated by decreasing the salinity during 1 to 2 hours followed by an artificial flood tide with gradually increasing salinity. The movements of the crabs were recorded over periods of 10 minutes as numbers of individuals passing an arbitrary vertical reference line, walking or swimming, either upstream or downstream. At an early stage in the experiments it already appeared that walking activities were of minor significance and did not show any relation to the stimuli introduced. Only the swimming response was found to be relevant. As has been pointed out before, the swimming power of the crabs has no significance for long-distance migration. The animals can hardly resist currents of 10 to 15 cm per second. As soon as the crabs
M I G R A T I O N OF S W I M M I N G C R A B
99
got off the bottom in the experimental channel they were inevitably transported around. The swimming activity or the rate of transport was measured by counting the numbers passing the vertical reference line per unit of time. Each crab persisting in swimming will, therefore, have been counted several times. The results are plotted in the diagrams of Fig. 3 together with the salinity and temperature changes. These diagrams provide good evidence that, when in a current of about 15 cm per second the crabs are subjected to decreasing salinity, they invariably respond by increased swimming activity. When, however, the salinity is increased again--which represents the beginning of the flood tide--swimming stops. This behaviour provides the swimming crabs with a reliable mechanism enabling them to avoid adverse salinities as soon as they occur, by the simple response of rising from the bottom. The tidal streams will then always carry the animals in the "correct" direction. This mechanism will undoubtly facilitate migration of swimming crabs out of the Wadden Sea when winter conditions occur. This implies that swimming activity released by salinity decrease will occur more readily in late autumn than, for instance, in summer. Temperature decrease alone--while salinity is kept constant--does not induce swimming activity (Fig. 35). The marked response of the swimming crabs when both salinity and temperature decrease (Fig. 3c, d and e) or when salinity decreases at a constant relatively low temperature (Fig. 3f, g and h) may suggest some interaction between these 2 factors in controlling the migration out of the Wadden Sea in late autumn. The data presented here, however, do not permit definite conclusions, and later attempts to establish such an interaction have hitherto been unsuccessful. V. D I S C U S S I O N
One of the characteristic features of Macropipus holsatus is its ability to swim by means of its specialized fourth legs, but the natatory mechanism is not sufficient for covering long distances. The swimming technique rather suggests its significance for occasional maintenance of a pelagic form of life during which the crabs are virtually subject to transportation by water currents. A natatory capacity is of widespread occurrence among the portunid crabs, and some species have been found swimming in large numbers close to the surface of deep water far from land (DELLA CROCE & HOLTI-IUlS,1964; ALLEN, 1968; HARTNOLL, 1971). It is difficult to evaluate the ecological significance of these swimming activities in open ocean conditions. In estuarine areas, however, the ecological significance of a selective use of either the flood or
100
S. G. VENEMA &F. CREUTZBERG
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MIGRATION
OF S W I M M I N G C R A B
101
the ebb tide as transportation medium in seasonal inshore and offshore migration is evident. The possibility that Macropipus holsatus might be able to distinguish between flood and ebb through its sensitivity to changes in hydrostatic pressure is discussed by MORGAN (1967). The experimental crabs appeared to perform movements with the swimming legs when subjected to sudden pressure changes corresponding to a 10 metre water depth, while the most sensitive of the animals responded to changes of 0.5 metre. The suggestion that these responses might be of depth-regulatory nature--although in M O R G A N ' S experiments responses to pressure decrease were observed as well--would explain a possible landward transportation on the flood tide. Off-shore transportation on the ebb, however, would rather, as suggested by MORGAN, be controlled by changes in temperature or salinity or both. In the present study evidence is presented that swimming crabs - - w h e n stationary near the bottom in an estuary--are responsive to salinity changes of the same order as occur during the incoming and outgoing tides. The tidal currents, apart from providing directional information about the salinity gradient, are utilized as a means of transportation as soon as the conditions become less favourable. A comparable salinity-controlled selective use of tidal currents in estuarine areas has been reported by HUGHES (1969) in the shrimp Penaeus duorarum in Florida's brackish waters. The question, however, of what mechanism is operative in the seasonal movements of Macropipus holsatus in and out of the estuaries is still unsolved. The suggestion that salinity-dependent swimming activity may be influenced by temperature has not been substantiated yet. The possibility that physiological and endogenous processes are involved in seasonally differentiated responsiveness to salinity changes must also be taken into account. In the pink shrimp Penaeus duorarum the postlarval stages which move into inshore waters show the reverse responsiveness to salinity changes of that exhibited by the juveniles or sub-adults, which move offshore (HUGHES, 1969), while the tideassociated migrations in this species appear to be controlled by an endogenous tidal rhythmicity as well (HUGHES, 1972). A more detailed study of the mechanism underlying the seasonal inshore and offshore migrations of Macropipus holsatus is therefore urgently needed. VI. SUMMARY
Macropipus holsatus, a common inhabitant of the North Sea, extends its geographic distribution into estuarine areas in spring, withdrawing
102
S. C. VENEMA & F . C R E U T Z B E R G
again in late autumn. These migratory movements were studied during fishery surveys carried out in the years 1961 through 1964 which showed that the distribution within the Wadden Sea is most probably determined by salinity. The migration of the swimming crab out of the Wadden Sea is controlled by tidal transportation triggered by a decrease of salinity. The possible mechanism underlying seasonal inshore and offshore movements is still unknown. VII. R E F E R E N C E S
ALLEN,J. A., 1968. The surface swarming of Polybius henslowi (Brachyura: Portunidae).--J, mar. biol. Ass. U.K. ,18:107-111. CREUTZBERO, F., 1961. On the orientation of migrating elvers (Anguilla vulgaris Turt.) in a tidal area.--Neth. J. Sea Res. 1 : 257-338. DELLA CROC~, N. & L. B. HOLTHUIS, 1964. Swarming of Charybdis (Goniohellenus) edwardsi Leene & Buitendijk in the Indian Ocean (Crustacea Decapoda, Portunidae).--Boll. Musei Ist. biol Univ. Genova 33 (199): 33-38. HARTNOLL, R. G., 1971. The occurrence, methods and significance of swimming in the Brachyura.--Anim. Behav. 19: 34-50. HUOHES, D. A., 1969. Responses to salinity change as a tidal transport mechanism of pink shrimp, Penaeus duorarum.--Biol. Bull. mar. biol. Lab. Woods Hole 136: 43-53. , 1972. On the endogenous control of tide-associated displacements of pink shrimp, Penaeus duorarum Burkenroad.--Biol. Bull. mar. biol. Lab. Woods Hole 142: 271-280. MOROAN, E., 1967. The pressure sense of the swimming crab Macropipus holsatus (Fabricius), and its possible role in the migration of the species.--Crustaceana 13: 275-280. POSTMA, H., 1954. Hydrography of the Dutch Wadden Sea.--Archs n~erl. Zool. 10:405-511. POULSEN, E. M., 1922. On the frequency and distribution ofCrangon vulgaris, Carcinus maenas and Portunus holsatus in the Danish coastal waters.--Meddr Kommn Danm. Fisk.--og Havunders (Fiskeri 6) 7: 1-18. , 1949. On the distribution of the Brachyura (Crustacea, Decapoda) in Danish waters.--Vidensk. Meddr dansk naturh. Foren 111: I 11-130. VERW~y, J., 1958. Orientation in migrating marine animals and a comparison with that of other migrants.--Archs n6erl. Zool. 13 (suppl.): 418-445. 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.-Neth. J. Sea Res. 5: 197-226.
SEASONAL MIGRATION OF THE SWIMMING CRAB MACROPIPUS HOLSATUS IN AN ESTUARINE AREA CONTROLLED BY T I D A L STREAMS by S. C. VENEMA* and F. CREUTZBERG (Netherlands Institutefor Sea Research, Texel, The Netherlands)
CONTENTS I. II. III. IV. V. VI. VII.
Introduction . . . . . . . . . . . . . . . . . . . . Hydrography of the Dutch Wadden Sea . . . . . . . . . . . . . . Fishery surveys. . . . . . . . . . . . . . . . . . . Mechanism of migration . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . Summary . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . .
. . . . .
. . . . .
. . . . .
. . . . .
. . . . .
94 95 95 97 99 101 102
I. I N T R O D U C T I O N The swimming crab Macropipus holsatus (Fabricius) is a common inhabitant of the open North Sea the whole year through, but in spring the animal extends its geographic distribution into estuarine areas, withdrawing again in late autumn. These movements have been reported by VERWEY (1958) for the Dutch Wadden Sea and by WOLFF & SANDEE (1971) for the estuarine area of the rivers Rhine, Meuse and Scheldt. In the present paper, the results of a study of these seasonal migrations, carried out during fishery surveys in the Dutch Wadden Sea in the years 1961 through 1964 in cooperation with our colleague M. Fonds will be given, as well as the results of laboratory experiments --carried out in 1962--on the possible mechanism underlying these migratory movements. Acknowledgement.--The authors wish to express their gratitude to Mr J. A. A. Spiekerman (The Hague) for correcting the English text. * Present address: Fisheries Resources Devision, Research Information Section, FAO, Roma, Italy.
MIGRATION
OF SWIMMING
CRABS
95
II. HYDROGRAPHY OF THE DUTCH WADDEN SEA The geomorphological structure of the Dutch Wadden Sea demonstrates the dominant role played by the tidal currents. According to POSTMA (1954) the distances covered by floats during a complete flood tide or ebb tide range between 10 and 24 km depending on the size of the tidal channels. Formerly the Wadden Sea and the Zuiderzee formed one open system. By the construction of the Afsluitdijk in 1931 the brackish Zuiderzee was gradually turned into a fresh water lake, the IJsselmeer. The salinity of the Wadden Sea, therefore, is mainly determined by the amount of fresh water discharged (at low tide) at the 2 sets of sluices located at both ends of the Afsluitdijk, with the result that the Wadden Sea is characterized by a salinity gradient ranging from about 18 ~oo near the A/'sluitdijk to approximately 30 ~o S in the tidal inlets between the islands (Fig. lf). In dry periods, when discharges of fresh water are stopped for some months, virtual marine conditions may occur in the Wadden Sea. Salinities vary greatly, with extreme differences being found near the Afsluitdijk. These variations are caused both by variations in the amounts of fresh water discharged by the sluices, and by tidal movements shifting the whole salinity gradient up and down. As for temperature, roughly similar types of gradients are observed in autumn, as a result of more rapid cooling of the shallow inland water than of the North Sea water in a period of decreasing air temperature. In spring, however, the salinity and temperature gradients show exactly the reverse picture, as a result of more rapid warming of the inland waters (PoSTMA, 1954). III. FISHERY SURVEYS In this area, monthly fishery surveys were carried out from October 1961 to October 1962 and from September 1963 to October 1964, using a 2½ metre beamtrawl and a I0 metre ottertrawl, respectively. All the catches were converted into numbers of animals per 1000 m 2. The distribution of swimming crabs appeared to be fairly regular through certain periods. This enabled us to average the catches made during selected groups of succesive months. The mean density of Macropipus holsatus in September, October and November 1963 at the different stations reveals that the swimming crabs show a preference for the outer area of the Wadden Sea and tend to avoid the brackish areas along the Afsluitdijk and the Friesland coast (Fig. la). The assumption that the furthest extent of penetration into a brackish area is determined by the decreasing salinity is also suggested by POULSEN (1922, 1949) for swimming crabs in the Kattegat area, where they are
96
S. C. V E N E M A
& F. C R E U T Z B E R G
not found in water of a salinity below 20 to 23 %0 S. WOLFF & SANDEE (1971) suggest a salinity not far below 27 %o as the limit of occurrence in the Rhine, Meuse and Scheldt estuary. There are indications that the salinity-dependent limit of occurrence in turn is influenced by temperature. In the winter months (December 1963 to March 1964) the crabs were found entirely or almost entirely withdrawn from the Wadden Sea (Fig. lb). Similar observations had been made in the winter of 1961 tot 1962. meon densily per I 0 0 0 rn= 0
I
•
2I0 II- 50 51- ;00 I01 - 2 0 0 201 - 4 0 0
•
4ol - 8oo
-,-,-
,o"1
,.
t~' e
Fig. 1. a-e. Distribution of Macropipuaholsatus in the western W a d d e n Sea expressed as numbers caught per 1000 m a over different seasons, f. Distribution of average surface salinity in 1962 in the western W a d d e n Sea.
M I G R A T I O N OF S W I M M I N G C R A B
97
Starting in April 1964, a gradual resettlement in the Wadden Sea took place, while again the extent of penetration appeared to be restricted to the more saline outer parts of the Wadden Sea during spring and early summer until June (Fig. lc). In August and September 1964, however, a remarkable extension of their distribution to the Afsluitdijk and the Friesland coast was observed (Fig. ld). Unfortunately our hydrographical data do not permit definite conclusions, but it is a fact that just prior to this time the fresh water discharges at the Afsluitdijk had been considerably reduced for some months. In October 1964 the more normal distribution was found again; discharges of the normal volume of IJsselmeer water had been resumed some time previously. Another slight indication of a salinity-temperature controlled migration is found in the distribution of swimming crabs in March and April 1962, during surveys which additionally covered a more eastern as well as more saline part of the Wadden Sea. While in the western (more brackish) part no swimming crabs were observed yet, immigration was already taking place in the eastern area (Fig. le). IV. M E C H A N I S M
OF MIGRATION
An incidental observation in September 1945 of large numbers of Macropipus holsatus swimming in the surface water during the ebb where few or none had been seen during the flood tide (VERwEY, 1958), gave rise to the assumption that the crabs use the tidal currents as a means of transportation in their seaward migration in autumn and supposedly also for inward migration in the spring. Since the swimming power of M. holsatus is negligible in comparison to the velocity of the tidal currents, swimming seems to have significance only in keeping the animal suspended in the water layers and probably the crab may well have no other means of migration than that of passive transportation. In the autumn of 1965 a series of attempts were made, using a pelagic trawl, to establish a seaward pelagic transportation of swimming crabs. In most cases, however, no pelagically-swimming crabs were caught, and when they were, the numbers were too small and too variable to demonstrate any differences between ebb and flood catches. These few results do not permit conclusions. The experimental approach to the problem was based on the supposition that during ebb tide a decrease of salinity acts as releasing factor for swimming behaviour. In the laboratory, therefore, the animals were subjected to conditions simulating ebb and flood tide by changes of salinity under constant current conditions. The apparatus used was a modification of the circular tidal stream apparatus (outer diameter 80 cm) designed for migration studies of young eels (CREuTZ-
98
S. C. V E N E M A
& F. C R E U T Z B E R G
BERO, 1961). In the modified arrangement the water-current-generating paddies are placed in the inner cylinder to avoid disturbances by moving objects in the experimental channel (Fig. 2). The circular current is admitted into the experimental channel through horizontal inflow r
~ J ~ _ _ ~ overflow
~
outer cylinder inner cylinder paddles
Fig.2. Circular tidal stream apparatus. open slits in the wall of the inner cylinder. An inflow in the inner cylinder and an over-flow in the outer cylinder maintain constant water renewal in the whole system. By changing the quality of the supplied water any characteristic of the water in the experimental channel, such as salinity and temperature, can be gradually changed to any extent. In each experiment usually 10 swimming crabs were placed in the experimental channel where they were allowed to burrow in the sandy substrate. Each experiment was introduced by a period of constant salinity and temperature for 15 to 60 minutes. Next an ebb tide was simulated by decreasing the salinity during 1 to 2 hours followed by an artificial flood tide with gradually increasing salinity. The movements of the crabs were recorded over periods of 10 minutes as numbers of individuals passing an arbitrary vertical reference line, walking or swimming, either upstream or downstream. At an early stage in the experiments it already appeared that walking activities were of minor significance and did not show any relation to the stimuli introduced. Only the swimming response was found to be relevant. As has been pointed out before, the swimming power of the crabs has no significance for long-distance migration. The animals can hardly resist currents of 10 to 15 cm per second. As soon as the crabs
M I G R A T I O N OF S W I M M I N G C R A B
99
got off the bottom in the experimental channel they were inevitably transported around. The swimming activity or the rate of transport was measured by counting the numbers passing the vertical reference line per unit of time. Each crab persisting in swimming will, therefore, have been counted several times. The results are plotted in the diagrams of Fig. 3 together with the salinity and temperature changes. These diagrams provide good evidence that, when in a current of about 15 cm per second the crabs are subjected to decreasing salinity, they invariably respond by increased swimming activity. When, however, the salinity is increased again--which represents the beginning of the flood tide--swimming stops. This behaviour provides the swimming crabs with a reliable mechanism enabling them to avoid adverse salinities as soon as they occur, by the simple response of rising from the bottom. The tidal streams will then always carry the animals in the "correct" direction. This mechanism will undoubtly facilitate migration of swimming crabs out of the Wadden Sea when winter conditions occur. This implies that swimming activity released by salinity decrease will occur more readily in late autumn than, for instance, in summer. Temperature decrease alone--while salinity is kept constant--does not induce swimming activity (Fig. 35). The marked response of the swimming crabs when both salinity and temperature decrease (Fig. 3c, d and e) or when salinity decreases at a constant relatively low temperature (Fig. 3f, g and h) may suggest some interaction between these 2 factors in controlling the migration out of the Wadden Sea in late autumn. The data presented here, however, do not permit definite conclusions, and later attempts to establish such an interaction have hitherto been unsuccessful. V. D I S C U S S I O N
One of the characteristic features of Macropipus holsatus is its ability to swim by means of its specialized fourth legs, but the natatory mechanism is not sufficient for covering long distances. The swimming technique rather suggests its significance for occasional maintenance of a pelagic form of life during which the crabs are virtually subject to transportation by water currents. A natatory capacity is of widespread occurrence among the portunid crabs, and some species have been found swimming in large numbers close to the surface of deep water far from land (DELLA CROCE & HOLTI-IUlS,1964; ALLEN, 1968; HARTNOLL, 1971). It is difficult to evaluate the ecological significance of these swimming activities in open ocean conditions. In estuarine areas, however, the ecological significance of a selective use of either the flood or
100
S. G. VENEMA &F. CREUTZBERG
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Fig.3. a-i. Number of swimming Macropi#us holsatus in the circular tidal stream apparatus passing an arbitrary vertical reference line over periods of I0 minutes (lower diagrams) together with salinity changes and temperature changes (upper and middle diagrams) during different trials.
MIGRATION
OF S W I M M I N G C R A B
101
the ebb tide as transportation medium in seasonal inshore and offshore migration is evident. The possibility that Macropipus holsatus might be able to distinguish between flood and ebb through its sensitivity to changes in hydrostatic pressure is discussed by MORGAN (1967). The experimental crabs appeared to perform movements with the swimming legs when subjected to sudden pressure changes corresponding to a 10 metre water depth, while the most sensitive of the animals responded to changes of 0.5 metre. The suggestion that these responses might be of depth-regulatory nature--although in M O R G A N ' S experiments responses to pressure decrease were observed as well--would explain a possible landward transportation on the flood tide. Off-shore transportation on the ebb, however, would rather, as suggested by MORGAN, be controlled by changes in temperature or salinity or both. In the present study evidence is presented that swimming crabs - - w h e n stationary near the bottom in an estuary--are responsive to salinity changes of the same order as occur during the incoming and outgoing tides. The tidal currents, apart from providing directional information about the salinity gradient, are utilized as a means of transportation as soon as the conditions become less favourable. A comparable salinity-controlled selective use of tidal currents in estuarine areas has been reported by HUGHES (1969) in the shrimp Penaeus duorarum in Florida's brackish waters. The question, however, of what mechanism is operative in the seasonal movements of Macropipus holsatus in and out of the estuaries is still unsolved. The suggestion that salinity-dependent swimming activity may be influenced by temperature has not been substantiated yet. The possibility that physiological and endogenous processes are involved in seasonally differentiated responsiveness to salinity changes must also be taken into account. In the pink shrimp Penaeus duorarum the postlarval stages which move into inshore waters show the reverse responsiveness to salinity changes of that exhibited by the juveniles or sub-adults, which move offshore (HUGHES, 1969), while the tideassociated migrations in this species appear to be controlled by an endogenous tidal rhythmicity as well (HUGHES, 1972). A more detailed study of the mechanism underlying the seasonal inshore and offshore migrations of Macropipus holsatus is therefore urgently needed. VI. SUMMARY
Macropipus holsatus, a common inhabitant of the North Sea, extends its geographic distribution into estuarine areas in spring, withdrawing
102
S. C. VENEMA & F . C R E U T Z B E R G
again in late autumn. These migratory movements were studied during fishery surveys carried out in the years 1961 through 1964 which showed that the distribution within the Wadden Sea is most probably determined by salinity. The migration of the swimming crab out of the Wadden Sea is controlled by tidal transportation triggered by a decrease of salinity. The possible mechanism underlying seasonal inshore and offshore movements is still unknown. VII. R E F E R E N C E S
ALLEN,J. A., 1968. The surface swarming of Polybius henslowi (Brachyura: Portunidae).--J, mar. biol. Ass. U.K. ,18:107-111. CREUTZBERO, F., 1961. On the orientation of migrating elvers (Anguilla vulgaris Turt.) in a tidal area.--Neth. J. Sea Res. 1 : 257-338. DELLA CROC~, N. & L. B. HOLTHUIS, 1964. Swarming of Charybdis (Goniohellenus) edwardsi Leene & Buitendijk in the Indian Ocean (Crustacea Decapoda, Portunidae).--Boll. Musei Ist. biol Univ. Genova 33 (199): 33-38. HARTNOLL, R. G., 1971. The occurrence, methods and significance of swimming in the Brachyura.--Anim. Behav. 19: 34-50. HUOHES, D. A., 1969. Responses to salinity change as a tidal transport mechanism of pink shrimp, Penaeus duorarum.--Biol. Bull. mar. biol. Lab. Woods Hole 136: 43-53. , 1972. On the endogenous control of tide-associated displacements of pink shrimp, Penaeus duorarum Burkenroad.--Biol. Bull. mar. biol. Lab. Woods Hole 142: 271-280. MOROAN, E., 1967. The pressure sense of the swimming crab Macropipus holsatus (Fabricius), and its possible role in the migration of the species.--Crustaceana 13: 275-280. POSTMA, H., 1954. Hydrography of the Dutch Wadden Sea.--Archs n~erl. Zool. 10:405-511. POULSEN, E. M., 1922. On the frequency and distribution ofCrangon vulgaris, Carcinus maenas and Portunus holsatus in the Danish coastal waters.--Meddr Kommn Danm. Fisk.--og Havunders (Fiskeri 6) 7: 1-18. , 1949. On the distribution of the Brachyura (Crustacea, Decapoda) in Danish waters.--Vidensk. Meddr dansk naturh. Foren 111: I 11-130. VERW~y, J., 1958. Orientation in migrating marine animals and a comparison with that of other migrants.--Archs n6erl. Zool. 13 (suppl.): 418-445. 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.-Neth. J. Sea Res. 5: 197-226.