Levin p. 2 ABSTRACT The marine snail, Littorina planaxis, has the ability to distinguish between solutions of high and low salinity. Research indicates that salinity is determined primarily through the detection of chloride. The region of de¬ teotion seems to be localized in the area, between the operculum and the foot, known as the operculigerous disc. Levin p. 3 INTRODUCTION Littorina planaxis, a gastropod snail, common to the upper intertidal regions of rocky coastal areas, is most often found with its operculum closed and attached to the rocks with a mucus seal. If a snail is dislodged from the rocks and placed into sea water it begins an extruding response, moving its operoulum away from the mouth of the shell and gradually extending its foot and tentacles. The extruding response consists of two parts. Stage one is a movement from a closed position to one where tentacles are exposed. Movement stops momentarily and the snail may reclose, or may continue with full ex¬ trusion of the foot, head, and tentacles. If a snail is dislodged and placed into distilled water, no stage one response occurs. Littorina planaxis must have some mech¬ anism that can determine certain properties of the sur¬ rounding water while the snail is drawn into its shell. The purpose of this research was to characterize this response and to localize the region of detection. Results suggest thatasnail detects primarily chloride concentra¬ tion. MATERIALS Littorina planaxis was collected from the rocks at the Hopkins Marine Station of Stanford University in Pacific Grove, California. Snails were either placed into distilled water or left to desiccate in dry wooden Levin p. 4 aquaria for several hours before each experiment. No snail was kept for more than 48 hours. Artificial sea water contained Nacl (450 mM), Mgcl, (50 mM), Cacl, (10 mM), KCI (10 mM), and Tris(hydroxy¬ methyl)aminoethane Hydrochloride (Tris HCl) buffer at pH 7.8 (10 mM). METHODS Standard testing procedure Each snail was removed from distilled water or from desiccation and placed with its operculum up. The oper¬ culum was then covered with 20 microliters of a test solu¬ tion, and the snail's response noted. A stage one response within two minutes was considered a positive response whether or not full extrusion occurred. No difference in response was ever noted between the two groups. No snail was tested more than once and responses from a group (4-2) of snails were combined to give a percentage of positive responses. All snails giving negative responses were then tested with artificial sea water (ASW) or natu¬ ral sea water (NSW) to make sure that the snails were alive. Characterization To determine the range of salinities over which the stage one response occurs, test solutions were made from ASW or from NSW. Test solutions were also made by add¬ Levin p. 5 ing varying amounts of Nacl, MgCl,, Cacl,, or KCl from 1 M stook solutions to a dilution of ASW at 200 mOsm to characterize the effects of different cations. lo test the effeots of anions, the following solutions were com¬ pared: 0.5 M sodium chloride, 0.52 M sodium D-gluconate, 0.5 M Tris HCI, 0.5 M and 0.4 M Tris citrate. All solu¬ tions were adjusted to pH 7.8 with either 5 mM Tris HCI buffer or NaOH. Non-electroyte test solutions con¬ tained sucrose adjusted to pH 7.8 with 10 mM Tris HCI buffer. Localization Mapping of regions sensitive to saline solutions was carried out by placing small amounts (1 to 5 micro¬ liters) of ASW or NSW on or around the operculum. To determine the role of the cephalic tentacles in the deteotion of salinity, it was necessary to remove these organs from a group of snails. An aqueous solu¬ tion of magnesium chloride isotonic with NSW was used as an anesthetic and relaxant (Peters, 1964). An immersion of 15 to 20 minutes was usually adequate to allow for easy removal of the tentacles. No long-lasting affeots of the anesthetic were ever apparent, even after immersions of two hours. Thirty snails were divided into three groups, an ex¬ perimental group, and two control groups. The experimental Levin p. 6 group was anesthetized in magnesium chloride, cephalic tentacles were removed, and the group was placed into normal sea water for recovery. One control group followed the same procedure except cephalic tentacles were not re¬ moved. The second control group was identical to the other control group except it was not placed into mag- nesium chloride. All three groups were placed into distilled water for 30 minutes prior to testing with NSW. Methylene blue stain (Loefflers) or one percent usec OsO, in 0.5 M sodium acetate wasito visualize those regions exposed to test solutions while the snail remained drawn into its shell. Snails were exposed to a stain either by placement of one drop of stain upon the closed operculum, or by direct immersion of the snail into the stain. Exposure time was varied. After exposure, snails were washed with distilled water, placed into isotonic magnesium chloride, and examined for stain¬ ed areas. RESULTS AND DISCUSSION Characterization The snails response to solutions of varying salin¬ ities is summarized in figure one. The graph is plotted as the percentage of positive sstage one) responses at a given osmolality of a test solution. NSW is around 970 Levin p. 7 mOsm. There are three possible methods that Littorina qualita planaxis might be using to determine the surrounding solutions: detection of total osmotic pres¬ sure, deteotion of ionic strength, detection of one specific ion. Of the twenty snails tested with sucrose solutions of 984 mOsm and 826 mOsm, all failed to give positive responses. The osmolalities of the sucrose solutions were well within a region that gave 100 percent posi¬ tive response with ASW and NSW. This result dees netsuppert the possibility that the deteotion of salinity is through the use of a general osmoreceptor. Results from additions of specific ions to the sub-threshold ASW dilution are summarized in figures two and three. In figure two, the percentage of positive responses is plotted against the percentage of a specific cation's concentration relative to the concentration of that cation found in ASW. A standard dilution curve for ASW is given as a reference. No positive responses ocourred with the dilution (arrow). If L. planaxis was testing for one specific ion, the curve for that cation should follow the dilution ourve of ASW closely. The data suggests that the snails are not testing solely for the calcium, magnesium, or potassium cation. The sodium Levin p. 8 ion is probably not the only stimulus for the extruding response either. There may, however, be some sort of summation of several ions to give a 100 percent positive response. No single cation gave 100 percent positive response except for Ca". As explained previously, Ca cannot be preferentially deteoted since its threshold for positive response is well above that found in NSW. A solution of Nacl with 10 mM Cacl, gave a curve similar to that of ASW. From this data either Na' or Cl appear to be pri¬ marily detected. Some concentration of Ca'* (between 2 and 10 mM) is needed for some snails to achieve a stage one response. At this point it is not entirely clear what the effeot of the calcium ion is. The data in figure two can be replotted as the per¬ centage of positive response against the concentration of the chloride anion (fig. 3). This graph shows a very steep function where a small increase in the chloride concentration results in a large increase in the per¬ centage of positive responses. As an example, the Ca curve rises from no positive responses to 100 percent positive response over only a 60 mM increase in chloride concentration. This comes close to resembling an on-off which set point, would be expected if salinity detection involved chloride only Levin p. 9 The results of the anion replacement tests also support the conclusion that Littorina planaxis responds to the concentration of chloride. Solutions of sodium chloride (n=8) and Tris HCl (n=6) both gave responses in over 80 percent of the snails. Test solutions of sodium D-gluconate (n=9), sodium phosphate (n=6), and Tris citrate (n=12) gave no positive responses. Localization Mapping of the opercular region indicates that the operculum itself is not sensitive to solutions of high salinity. The extruding response does not occur unless the solutions come into contact with the crack between the operculum and the shell. Further localization was achieved through staining experiments. In all cases (n=25) the only stained region was the area lying between the foot and the operculum, the operculigerous disc (Fretter & Graham, 1962). Even after immersion of one hour in methylene blue, no other areas showed signs of staining. It should be noted that OsO)--Acetate stained similarly, did not give a stage one response,did not kill the snail. Removal of the cephalic tentacles had no effect upon the extruding response (n=10). Further operations were performed by removing the operculigerous disc. After a Levin p. 10 twenty-four hour recovery period snails were tested with NSW. No difference was noted in the extrusion response between experimental (n=14) and control (n=6) groups. Snails were then allowed to recover for an additional 24 hours, afterwhich half were tested with a dilution of 60 percent ASW and half with sodium D-gluconate. Response to the dilution was slowed (n-3) or absent (n-4) among the experimental group. Response was 100 percent among the controls (n=3) and among snails previosly tested with dilutions at and slightly below the 60 percent test solu¬ tion (n=13). No difference in response was noted between experimental (n=7) and control (n=3) groups in response to sodium D-gluconate. Thus, destruction of this region does have an effect upon the snail's ability to deteot salinity. At this point it is unclear why removal of the dise should have little affect upon the detection of NSW, but have a large effect upon the detection of a dilution. Previous research (Kohn, 1961) also suggests that this region is the primary site of detection in an¬ other species, Nodilittorina granulus (Gray). In summary, Littorina planaxis has the ability to determine the concentration of chloride in solution while the snail is drawn into its shell with its operculum closed. The calcium cation appears to have some small, Levin p. 11 unclear effect as well. The region between the foot and the operculum appears to be the primary region of detec¬ tion as determined by staining and direct removal of the area. ACKNOWLEDGEMENT I wish to thank Dr. William F. Gilly for his tremen- dous assistance and patience throughout the course of this research. Levin p. 12 REFERENCES Berger, V. Ja., 1978. Comparison of the adaptations of mollusks to extreme and moderate changes in salinity. Mal. Rev., Vol. 11, pp. 110-111 Fretter, V. & A. Graham., 1962 British prosobranch molluses . Ray Society, London, 75 pp. Kohn, A. J., 1961. Chemoreception in gastropod molluscs. Am. Zoologist, Vol. 1, pp. 291-308 Peters, R. S., 1964. Function of the cephalic tentacles in Littorina planaxis Philippi. Veliger., Vol. 7:2, pp. 143-148 Stephens, P. J., 1978. The sensitivity and control the scallop mantle edge. J. exp. Biol., Vol. 75, pp. 203-221 C Figure One The percentage of positive (stage one) responses is plotted against changing osmolalties. Normal sea water is around 970 mOsm O N 9 8 osuoase isod % 9— t H t H H O Figure Two The percentage of positive responses is plotted against the percent concentration of a specific cation in the test solution as comparaed to its normal concen¬ tration in ASW. As an example, a 60 mM Cacl, test solution yielded 25 percent positive response. The normal concentration of Cacl, in ASW is 10 mM. The respective plot for this point is at (600,25). Activity coefficients were not considered and are implied to be one at all di¬ litions. The arrow represents the ASW dilution (see also text). o — 5 300 S S - 8 kevity wusdrech and e weplit tu wettiert wed at a all diluli H ++ H H 1 O O O C a Figure Ihree The percentage of positive responses is plotted against the concetration of chloride in millimolar units. he cation indicated refers to the major species with which the chloride ion was being added to test solutions. 8 0 — - — 8 100 75 50 25 N-252 — 0 0——0 Cat A—Mg D Na Na with — O mMolar Cacl 9 — — Li 100 200 300 400 500 600 concentration of CI (mM) .. C N-252 &am C +++