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6.3 THE ADAPTATION OF GUNDA ULVAE TO SALINITY I. THE ENVIRONMENT BY C. F. A. PANTIN, MA. (From the Zoological Laboratory, Cambridge, and the Marine Biological Laboratory, Plymouth.) (Received ist October, 1930.) (With One Text-figure.) WHEREAS it is well known that most organisms cannot survive sudden large changes in the salinity of the external medium yet estuarine organisms have developed powers of resistance to them. Recent work, particularly that of Schlieper (1929), has thrown some light on the behaviour of estuarine animals in diluted sea water. In most estuarine animals the salinity variations of the environment fall far short of the change from completely fresh water to undiluted sea water. But the triclad worm, Gunda ulvae, is found where variations of this magnitude may be expected with each tide, for it inhabits the sea shore at the estuaries of very small streams. The ability of these worms to withstand these changes is the more remarkable because of their small size, and because they are not covered with a protecting cuticle which might render them impervious to environmental osmotic changes. Moreover, whereas coelomates may mitigate the effect of such changes upon their cells by control of the composition of their body fluids, Gunda possesses no body cavity. Salinity variations may be expected to influence greatly the water exchange of Gunda, and experiments showed that this was true (Weil and Pantin, 1931; Pan tin, 1931). But it was soon found that in order to interpret these experiments an accurate description of the environment was required. Little attention has yet been paid to the immediate physical and chemical environment in which an estuarine organism lives. Thus, although Gunda lives definitely in association with fresh water, it seems possible that by suitable changes of position it might avoid gross changes in salinity. Reid (1930) found that in a small stream flowing over a sandy shore water deep in the sand may retain a fairly high salinity at low tide. It is therefore necessary to determine the exact distribution of the Gunda and the salinity variations in its neighbourhood. 64 C. F. A. PANTIN Further, experiments on the salt exchange of these worms when exposed fresh water showed that the chemical composition of this water was a factor of prime importance. The mere description of salinity changes is inadequate: the problem of estuarine existence is not one of simple dilution but of dilution accompanied by changing chemical composition, a factor which may vary in every river. Indeed, when speaking of estuarine conditions, the term "fresh water" is far too wide, .and may cover waters which differ among themselves almost as much as any of them do from sea water. It was therefore necessary to determine the composition of the water flowing by the Gunda in their natural habitat. THE MEDIUM. Gunda ulvae is found in large numbers in the estuary of a small stream at Wembury (South Devon) where this flows over an open foreshore. It is not found except in association with both fresh water and sea water. The external medium consists entirely of mixtures of stream water with Atlantic sea water. The following methods were used to analyse the stream water. A large sample of stream water was collected on July 23rd, 1930, and the following constituents determined: (1) Total solids, by evaporation to dryness on a water bath, followed by heating to 1800 C. to constant weight. (2) Carbonates, by titration while boiling with H2SO4 to/>H 7, using phenol red. (3) Chlorides, by titration by Mohr's method with AgNO3 (Treadwell and Hall, 1928). (4) Sulphates, determined as BaSO4 using the turbidimetric method of Thresh and Beale (1925). (5) Calcium, by conversion to oxalate and titration with KMnO4 (Treadwell and Hall, 1928). (6) Magnesium, determined as phosphate in the nitrates from (5) using the turbidimetric method of Thresh and Beale (1925). (7) Sodium andpotassium, by removal of SO4, Mg and Ca; conversion to chloride, and the dry weight compared with the AgNO3 titre. The method estimates accurately the total alkali metals present but does not give accurately the proportion of Na to K. The exact determination of this was not considered necessary. Four sets of independent determinations of each constituent were made. The maximal and minimal values found'are shown in Table I. The stream water is a typical hard water containing in addition to CaCO3 a large amount of Mg and SO4. The high alkali chlorides probably result from the cultivation of the land through which it flows. In winter the Cl' rises and the CO 3 " falls (column 4). The change in salt concentrations is, however, far smaller than the change in volume of water in the stream. The other component of the mixture in the estuary is Atlantic sea water, the composition of which is shown in Table I. This was calculated from Dittmar's (1884) analysis. The Adaptation of Gunda ulvae to Salinity Table I. Milligrammes per litre. Wembury stream water Atlantic sea water calculated from Dittmar (1884) July 23rd, 1930 co3 Cl so Ca4 Mg Na K Sum Total solids found *H Maximum Minimum 1194 41-3 24-6 647 14-4 1188 918 408 50-0 24-3 — 632 3085 291-4 3*9 317 58-4 — — — — — — 77 246 I9S 78 13-9 17-5 129 0073 19-64 2-69 0-42 131 10-70 0-39 35-22 x 10s x io 3 xio* x 10s xio3 xio3 xio3 xio3 — 82 HABITAT. Gunda is found under stones in the estuary of the Wembury stream. It is rarely found beneath stones less than 15 cm. in diameter, probably because these are subject to violent movement in rough weather. The stream itself rises in the Staddon grits and flows over Middle and Lower Devonian slates and grits. The basin is about 2 miles long and contains much cultivated ground. The stream flows rapidly and varies considerably in volume according to the season. In July 1930 it was roughly 1 to \\ m. in width and 10-15 c m - deep at the mouth. It may reach many times this volume in winter. It debouches into a fresh-water pool (about 5 m. x 25 cm. deep) at the top of a beach of shingle (Fig. 1) in Wembury Bay. Beyond the pool is a shelf of shingle thrown up by the highest tides. The shingle consists of stones averaging 3-5 mm. in diameter, together with larger stones and boulders. The stream cuts through this " beach shelf" and flows rapidly down to the edge of the shingle (Station E, Fig. 1). In the next section (Stations E-M) it flows through channels and pools in the rocks with some fine shingle and large stones in its bed. Beyond Station M (Fig. 1) the stream flows between rocks and sand. The bed of the stream in the middle section of the estuary (Stations E-M) is fairly constant. But the course through the shingle varies greatly in rough weather, and much of the water in this region flows through the shingle and not on the surface. Thus, from July 15th to 19th, 1930, the stream flowed from the pool over the shingle, decreasing to about one-half of the volume on the land above the pool; reappearing full-size round Station E. The sea was calm and the bed of the stream fairly constant. From July 28th till August 1st the stream disappeared into shingle at the end of the pool, reappearing as several small springs 10-20 m. down the beach. The sea was then rough, and the shingle altered each tide. JEB-VIIli S 66 C. F. A. P A N T I N Observations were made in the fresh-water pool, P, and at Stations A-]VH extending down the estuary to a point beyond the occurrence of Gunda. The levels and distances of the more important stations were surveyed for me by Mr M. A. Spender. These are shown in the vertical section in Fig. i, together with the heights of tides. T h e latter are based on the Devonport Chart Datum for tides in the Hamoaze. The observed tides at Wembury agreed well with these except that, when the sea was rough on July 28th, 1930, large breakers swept above the level of high-water spring tides and entered the fresh-water pool. Fresh-water pool Lowest record ol freshwater fauna, July 1930: Level of beach sheU. Desert region Upper limit of Ounda and Pntoiribu Upper limit of Enteromorpha • Lower limit of Gunda and I Pmtodrilu* 40 /•» /"» r\ -Shingle / / / / / « Bock + boulders 50 60 80 90 100 1 10 Metres below pool (measured along bed of stream) Density of Gunda population along stream Fig. i. Vertical section along estuary of stream, showing substratum and limits of organisms, etc. At spring tides, July 28th, 1930, fresh-water fauna pushed back to pool, and upper limit of Gunda at Station D. The fauna showed a regular sequence from a very rich fresh-water fauna in the pool to a normal marine shore fauna. The following collections made are typical. FRESH-WATER POOL P. Platyhelminth.es Hirudinea Gastropoda Crustacea Insecta Polycelis cornuta1 Glossosiphonia heteroclita Herpobdella atomaria Rissoa ventrosa Gammarus pulex Larvae of Ephemerida; Plecoptera; Chironomidae; Trichoptera 1 This organism agrees perfectly with the description (Whitehead, H., 1921), although it has been suggested that it is restricted in habitat to high land in a manner similar to Planaria alpina (Hubault, 1927). The Adaptation of Gunda ulvae to Salinity STATION B. Nil. STATIONS C AND D. Platyhelminthes Archiannelida Gunda ulvae Unidentified Acoelan Protodrilus flavocapitatus STATIONS E, F, G AND H. Platyhelminthes Archiannelida Crustacea Gunda ulvae Protodrilus flavocapitatus Gammarus sp. (undescribed) Jaera marina STATION K. Coelenterata Platyhelminthes Archiannelida Gastropoda Crustacea Actinia equina (one small specimen) Gunda ulvae Protodrilus flavocapitatus Patella vulgata (very few) Gammarus sp. (undescribed) Melita palmata Jaera marina STATION L. Coelenterata Platyhelminthes Gastropoda Crustacea Vertebrata Actinia equina Gunda ulvae (one specimen found on one occasion only) Craspedochilus cinereus Patella vulgata Gammarus sp. (undescribed) Melita palmata Jaera marina Sphaeroma serratum Carcinus maenas Onos mustelus STATION M. As Station L; no Gunda found on any occasion. The estimated population density of Gunda is shown in Fig. 1. It will be seen that the fauna falls into well-defined regions: I. The fresh-water fauna of the stream and pool. This usually ceases at P, but during the calm weather and neap tides, July I5th-i6th, 1930, it extended down to A. II. A desert region devoid of fauna extending roughly from high-water level of spring tides to high-water level of neap tides (Stations A-C). III. A region containing only a poor fauna of Gunda, Protodrilus and an Acoelan worm (only found July 15th, 1930). This region extends from high-water neaps to the lower edge of the shingle (Stations C-E). IV. A region containing Gunda, Protodrilus, Jaera and Gammarids (Stations E-K), extending from the edge of the shingle to low-water neaps. 5-2 68 C. F. A. PANTIN V. A region where a typical marine shore fauna is established, with Gunda' absent, extending from just below low-water neaps out to sea. Gunda occupies Regions III and IV. The upper limit of the range of Gunda in Region III varies considerably. During the calm weather and neap tides of July i5th-io,th, 1930, the range extended to Station C, that is, to within a metre of high-water neap tide level. On the other hand, during the rough weather and spring tides of July 28th-August 1st, 1930, the desert region extended further down, and few Gunda were found even at Station D. This desert region is so striking that it merits discussion. The poverty and variable limits of the fauna below this in Region III seem to be associated with the fact that it is composed of shingle, which shifts in rough weather. The desert region itself may lack a fauna, partly because of the intensity of mechanical disturbance to which it is subjected and, in the case of Gunda, because of the inconstant bed of the stream at low tide. But these factors cannot completely account for the absence of fauna, since Region III, which contains Gunda, is equally subject to mechanical disturbance. It is significant that this desert region corresponds roughly to the region between high spring and high neap tides. Such a region which is only at long intervals or irregularly subject to the presence of sea water is clearly a most rigorous environment, and these conditions may well prevent encroachment of Gunda into this region apart from the difficulties associated with mechanical disturbance. In the same way, the occasional incursions of sea water undoubtedly prevent the fresh-water fauna from moving downwards. Thus, on July 19th, 1930, during calm weather and neap tides, the fresh-water fauna had encroached on the desert region down the stream below the pool, and was only limited at Station A, which was below the level of high spring tides. By July 28th, 1930 (morning) the spring tides and greater reaching power of the waves had driven the fresh-water fauna back to the pool, P. The evening tide of the same day was the highest of the month and the sea was so rough that large .waves entered the pool at high tide. The fresh-water fauna rapidly disappeared from the pool. By August 1st, 1930, however, the tides were receding, the weather calmer, and the fresh-water fauna had re-established itself in the upper half of the pool, the water of which was now fresh to the taste. On its upper side the desert region thus seems to be defined by the tendency of the fresh-water fauna to encroach downwards, the encroachment being limited by incursions of sea water during high spring tides and rough weather. At other times, particularly during neap tides, the downward movement is favoured by the fact that at the upper edge of the tidal range the salinity may still be locally very low, and is rapidly reduced as the tide retreats. Moreover, the fresh-water organisms can withstand some concentration of sea water. Experiments on Polycelis cornuta immersed for 24 hours in different dilutions of sea water showed that it could withstand up to 6 per cent, of sea water for this period. The Adaptation of Gunda ulvae to Salinity 69 But although some fresh-water organisms can withstand a small concentration of sea water, and although some marine organisms such as Gunda can withstand fresh water for a time, yet the desert region provides a real division between what is only a modified marine fauna and what is a true fresh-water fauna. No organisms were found which could not definitely be assigned to one or other of these. Throughout the rocky Region III Gunda is present in large numbers. The bed of the stream here is permanent, depending on the shape of the rocks themselves. Gunda ceases to be found within a few metres of low-water neap-tide level: moderate numbers were found at Station K, but only one was found on one occasion at Station L, 5 m. beyond. None were found at Station M. This same limit was maintained both at neap tides and at the spring tides, July 28th-August 1st, 1930. Salinity measurements indicate that the factor in this case may be the insufficient dilution of the sea water by fresh water at low tide. It was remarkable that, although Protodrilus, which behaves in a manner similar to Gunda with respect to salinity changes (Weil and Pantin, 1931), was found in moderate numbers over almost exactly the same range as Gunda on July 15th19th, 1930, none of these were found at all on July 28th, 1930, and one near low-water neaps on August 1st, 1930. Clearly some other unknown factor also controls the distribution of Protodrilus. It must, therefore, be carefully borne in mind that in Gunda itself factors not recognised in these papers may also control its distribution, and that this description of its environment must be held to apply rigidly only to the period when observations were made, the month of July 1930. SALINITY. The salinity changes of the environment were determined by measurement of the electric conductivity of the medium. Samples were taken over the region of the distribution of Gunda. Their resistance was compared with artificial dilutions made from one particular sample of sea water taken well clear of the stream mixed with stream water taken about 300 yards inland. In comparison with this sample of sea water English Channel sea water taken several miles from the coast had a conductivity of 103 per cent. Since the water of the stream contains a large proportion of salts it has a fairly high conductivity, approximately equal to that of a 0 7 per cent, solution of sea water in distilled water. With proper temperature control the presence of o-oi per cent, of sea water in the river water can be measured. All measurements were made at 16-5° C. The following observations show that the water in immediate contact with the Gunda must vary from undiluted sea water to water in which the amount of sea 70 C. F. A. PANTIN water is negligible in comparison with the amount of salts already in the fresh water. July 15th, 1930. STATION E. Low tide: 3.30 p.m. Sea water (% 0-03 3.30 p.m. Surface water 0-03 Under stone with Gunda ... 0-07 12 cm. below stone in shingle High tide: 10.0 a.m. 12.20 p.m. (Station under 50 cm. of sea water and 3-4 m. from water's edge) 100 Surface water 100 Under stone with Gunda ... 5 cm. below stone in shingle 95 The samples were taken by inserting a pipette under stones beneath which it was supposed Gunda would be found, the presence of the latter being ascertained after the sample was taken. The deep samples were taken in order to determine the presence or absence of any water of very different salinity in the neighbourhood of the Gunda. Table II shows the successive changes in salinity during a single tide at six stations down the estuary. It is evident that the range covers enormous salinity variations. At the upper end the worms are subject to a small percentage of sea water for perhaps an hour each tide. At the lower end of the range they are under normal sea water for some 7 hours, and during the remaining 5 hours the sea water may fall to about 10 per cent, of the normal concentration. In the maximal part of the range the salinity varies from almost completely fresh water to undiluted sea water with each tide. It is apparent that Gunda is normally called upon to make full use of any powers it has to withstand salinity changes. Indeed its occurrence becomes rare as soon as these changes become reduced in magnitude (e.g. at Station L, just below low-water neaps). This is remarkable because Gunda can be kept alive for months in undiluted sea water, though experiments indicate (Pantin, 1931) that these conditions impair for a time their ability to withstand osmotic changes. The general problem of adaptation to estuarine conditions is, therefore, presented in a most striking form by Gunda ulvae. A study of the physiological mechanisms concerned in such a case as this may be expected to yield more information as to the means by which marine forms during evolution become adapted to fresh-water existence than may be gleaned from most estuarine organisms, which never come in contact with purely fresh water. Gunda can behave temporarily as a fresh-water organism: why is it still sufficiently dependent upon sea water to prevent its range extending into a purely fresh-water environment? In the succeeding papers an attempt is made to analyse the physiological changes induced in the worms on transference from marine to fresh-water conditions. The Adaptation of Gunda ulvae to Salinity Table II. High tide: 11.50 a.m.; 12.0 midnight. Low tide: 6.0 p.m. July 19th, 1930. Station Distance below pool (m.) Height above low-water springs (m.) C 165 43 D 230 38 Time f. h. e. 10.30 a.m. 11.50 2.15 p.m. 1f. f. 5-55 8.40 9.55 a.m. f. h. E G K L 33'O 460 78-0 84-0 30 2-4 17 1-2 10.40 11.45 e. 1.45 p.m. e. 2.30 1f. 5-5° 8.40 f. h. e. 1f. f. 10.15 a - m 11.50 2.40 p.m. 5-45 8.35 9.00 e. e. 1f. e. e. 1 Je. 'if. f. e. 2.45 p.m. 3-iS 5-4° 8.30 3.30 p.m. 4-55 5-35 6.30 8.30 3.30 p.m. Sea water (%) Sea water (%) in surface 8 cm. in shingle water o-oo O'OI 3-2 0-16 003 000 001 o-oo 004 0-04 860 IOI-O 072 0-03 o-oo O'OI 001 050 830 24-0 005 003 0-05 83-0 940 1030 IOO-O 3-i 3S-° o-oi o-oi 0-04 0-05 23-0 99° 92-0 25-0 91-0 280 0-56 90-0 73-o 870 ioo-o IOO-O 260 43-0 67-0 6i-o 80 7-4 l.ff|f. 5.00 30 I"6.20 ioo-o ioo-o 78-0 i. 8.30 6i-o ioo-o e. 001 139 IOO-O IOO-O 090 720 810 IOO-O C corresponded to the upper limit of Gunda. D was in the shingle zone (III). E on the upper border of the rock zone (IV). G on the rock zone (IV). K at the lower limit of Gunda, and L 6 metres beyond K. f.=flood; h. = high tide; e.=ebb; l.=low tide. SUMMARY. 1. The environment of the triclad Gunda ulvae has been studied. This organism lives on the sea shore in the estuaries of very small streams. 2. The components of the external medium are (a) stream water, which is rich in Ca and C0 3 , and (b) Atlantic sea water. These are mixed in different proportions in different parts of the estuary. 3. An analysis of the stream water is given. 4. The habitat of the organism is described. This extends roughly from highwater neap tides to low-water neap tides. A faunistic survey is given. 72 C. F. A. PANTIN 5. The conditions which control the limits of the habitat of Gunda are discussed. Between the upper limit of occurrence of Gunda and the place of occurrence of fresh-water forms there is a region devoid of fauna. This region corresponds roughly with the span between high-water neap tides and high-water spring tides. 6. Salinity determinations have been made on samples taken from the actual places where Gunda occurred. It is shown that Gunda has to withstand changes from completely fresh to undiluted sea water. It may normally be exposed to either extreme for several hours. 7. Salinity determinations made continually throughout the range of Gunda show that its environment may vary from one in which it is subjected to the action of sea water for only about 1 hour at high tide to one in which the sea water is only diluted to about 10 per cent, of its normal strength for a few hours during low tide. I wish to thank most gratefully Mr G. A. Steven of the Marine Biological Laboratory, Plymouth, for his assistance in the identification of organisms, and Mr M. A. Spender who very kindly surveyed the estuary of the stream for me. I also wish to thank the Staff of the Marine Biological Laboratory, Plymouth, for the many facilities with which I was provided. REFERENCES. DITTMAR, W. (1884). Challenger Report, Physics and Chemistry, 1, 203. HUBAULT, E. (1927). Inverttbre's Torrenticoles. Paris: Dulau & Co. PANTIN, C. F. A. (1931). Journ. Exp. Biol. 8, 82. REID, D. M. (1930). Journ. Marine Biol. Assoc. 16, 609. SCHLIEPER, C. (1929). Zeit.f. vergleich. Physiol. 9, 478. THRESH, J. C. and BEALE, J. F. (1925). The Examination of Water and Water Supplies. 3rd ed. London: J. and A. Churchill. TREADWELL, F. P. and HALL, W. T. (1928). Analytical Chemistry, 2, 7th ed. John Wiley and Sons, Inc. WEIL, E. and PANTIN, C. F. A. (1931). Journ. Exp. Biol. 8, 73. WHITEHEAD, H. (1921). Essex Naturalist, 20, 1.