ACKNOWLEDGEMENTS Special thanks to Dr. D.P. Abbott for his dedication to providing a unique and personal learning experience for students. Also, thanks to Chuckand Robin for both their scientific and spiritual contributions to my project. In general, thank you to the entire Hopkins Marine Station staff and class; though this spring was a rigorous and sometimes trying experience, it was indeed pleasant and worthwhile. a 2 I. Introduction Investigations on planktonic copepods and other open water crustaceans have shown that in some species phototaxis is affected by various environmental conditions such as salinity (Loeb 1893, Rose 1925 in Waterman 1961), oxygen tension (Herter 1927 in Waterman 1961), pH (Loeb 1906 in Waterman 1961), temperature (Dice 1914, Loeb 1893, Rose 1925 in Waterman 1961) and turbulence (Herter 1927 in Waterman 1961). Tigriopus californicus is an abundant copepod found along the California coast in high splash pools. These pools often remain out of communication with the open ocean for extended periods of time, and undergo large fluctuations in salinity, oxygen and pH (Burnett 1977, pers. comm.). In the face of these extreme conditions, the survival of the animal may be enhanced by the ability to exhibit different responses under different environmental conditions. This would include responses to such stimuli as light and gravity. No previous work has been published on the phototactic responses of Tigriopus californicus. Vertical movement is of particular interest since most environmental parameters such as salinity, oxygen, etc. exhibit vertical gradients in the habitat. This being the case, vertical movement is more likely to bring about a change in local environment than a horizontal one, and thus be the most adaptive short term strategy. In the long term, habituation or acclimation may occur. The following study examines short term upward and downward motion of Tigriopus californicus associated with an abrupt change in salinity, oxygen tension or pH, under a constant directional light source. II. General Materials and Methods The animals were collected from one high tidepool at Mussel Point, Pacific Grove, CA. A suction bulb was used to obtain a sampling from all portions of the water column, and the animals were strained through a nylon netting which passed larvae but held the larger adults. The animals were collected daily to avoid abnormal behavior cause by unnatural or stressful laboratory conditions. Only females with egg sacs were used in the study to avoid possible variability due to sex and age. In all experiments, "normal" conditions (as of temperature, salinity, oxygen, pH, etc.) are defined as those found in the running sea water system of Hopkins Marine Station fed by bay waters (see fig. 2). The physical set-up used in all experiments is diagrammed in figure 1. A series of 5 to 9 50ml graduated cylinders was placed above or below the directional light source; each cylinder contained sea water, 12cm deep, with one experimentally adjusted parameter. Twenty females with egg sacs were sucked into a narrow tube (inside diameter = 0.3cm) along with enough "normal" sea water to form a column of water 12cm long. With its upper end closed by a finger, one such tube containing 20 animals was gently lowered into each cylinder until its lower end rested on the bottom of the cylinder. The tube and cylinder were allowed to sit this way for 30 minutes. The 30 minute equilibration period was chosen as a time for which the difference between normal conditions within the tube and its surrounding cylinder could be maintained, yet allow the animals maximal time to adjust to the light conditions and erase any memory of turbulence or light-dark history. In most cases the base of the inner tube fitted tightly enough against the bottom of the graduated cylinder to prevent significant exhange of fluid or premature escape of Tigriopus. In the few cases where the animals did escape, the results were not used in calculating mean movements. At zero time the number of copepods in each 3cm segment of the inner tube was recorded; then the animals were released from the inner tube to the environment of the cylinder by slowly pulling the tube out of the cylinder. Two minutes later the number of animals in each of four 3cm segments of the cylinder was recorded. The copepods usually showed marked short term changes in vertical distribution. Shorter exposure times gave more variable results. For exposures greater than 5 minutes (depending on the condition) the animals showed a grend toward random vertical distribution. This system offers various advantages and disadvantages. It attempts to mimic a possible realistic situation in which the animal swims into some new local environment and experiences a change in some environmental parameter. It allows manipulation of some parameter without confusing its effects with those of turbulence or a change in light. A dual control is provided by this test. First, for each tube, the zero time count provides a normal environmental control contrasting with the 2 minute experimental value. Secondly, a normal control is included near the middle of the test range, where no environmental change occurs upon the animals' release from the inner tube. III. Changes in Vertical Distribution with a Sudden Change in Salinity under a Constant Directional Light Source The salinities tested ranged from 1Oppt to 110ppt, approximately 1/3 to 3 times normal sea water. All salinity solutions except normal (34ppt) were made up with Instant Ocean sea salts and tap water. The parts per thousand of each solution was determined by an American Optical Co, refractometer calibrated for salinity determinations. In the high salinity tests the "normal" salinity water tended to rise to the surface. Occasionally copepods entered this layer and stayed there. Therefore, after raising the inner tube the top one milliliter was aspirated off the water column of the cylinder to eliminate a less dense, normal salinity layer as an alternate environment to the test condition of the rest of the cylinder. Removal of a possible denser normal layer on the bottom of the low salinity tests was not possible without introducing disruptive turbulence. A. Responses to Changes in Salinity with a Constant Light Source from Above The results of four separate trials are shown in Table 1. In all trials, regardless of the time of day they were carried out, some consistent trends are observed, justifying combining the data sets to yield a composite picture of the response, shown numerically in Table 1, graphically in fig. 3. The trends are as follows: 1) Counts taken before the animals were released into the test condition show no marked tendency for the animals to be in either upper or lower half of the column. 2) Upon encountering low salinities (lOppt - 25ppt) the animals tend strongly downward, away from the light, resulting in most of the animals occupying the bottom quarter of the column. 3) Upon encountering high salinities (80ppt - 110ppt) the animals tend strongly upward, towards the light, resulting in most of the animals grouped in the top quarter of the water column. 4) In the intermediate salinity range (34ppt - 60ppt) there is a small shift downward. This behavior seems quite adaptive. If it is advantageous for an animal to avoid high or low extremes of salinity it should swim downward on encountering lower salinities since the denser, higher salinities would be found towards the bottom; conversely, upon encountering a higher salinities an animal ought to swim upward, the most likely direction of a lower salinity. In a tidepool in the field, two major stimuli provide cues as to the directions up and down. Light always enters from above the horizon, ranging from near horizontal to directly above. Gravity provides another cue as to the directions up and down. In the above experiments, at low salinity, Tigriopus show a negative phototaxis and a positive geotaxis. At high salinities they «how a positive phototaxis and negative geotaxis. At unusually low and high salinities the physical properties of the medium itself would tend to reinforce the above taxes; animals neutrally buoyant at a given salinity would tend to sink down in the less dense water at lower salinities and float upwards in the denser water at high salinities. Such physical response may contribute slightly to the foregoing results, but does not explain them as will be seen in the next experiments. The experiments with light from above offer no clue as to what environmental cues Tigriopus is using to distinguish up from down. One approach to separating the effects of light and gravity is to experimentally provide illumination from below instead of from above. If the response of Tigriopus is made mainly on the basis of gravitational cues, the vertical distribution of copepods should not change from that seen in the experiment with light from aboye. If light provides the major directional cue, a reciprocal distribution would be generated. If both cues are operating strongly, some intermediate results would be expected. B. Responses to Changes in Salinity with a Constant Light Source from Below In all three triabperformed, the animals moyed toward the bottom of the tube at all salinities, though the tendency is weakest at both high and low salinity extremes (Table 2, fig. 2). A row-by-column contingency test indicates that the distribution found at these extremes is significantly different from the distribution at the intermediate salinities to a confidence level of p.005. The results at the extremes immediately dispel any possibility that buoyancy effects are a major factor, since eyen at the densest salinity animals can be found on the bottom, and even at the lowest salinity animals can be found at the top. The results also cannot be explained by response to gravity or to light alone. Usually at high salinities the adaptively advantageous behavior should be to swim upward, reflecting a negative taxis to gravity and a positive taxis to light. With illumination from below, light and gravitational cues are contradictory. Adaptively speaking the animals should have moved upwards yet they are found on the bottom, so light must be exerting a stronger directional effect than gravity. At low salinities, the adaptive response should be to swim down; normally this means away from light and toward gravity, but here again with light from below, the cues conflict. More animals swam down than up, so perhaps the gravitational cue here is the more important. However, the tendency to go down is much less clear cut here than in experiments with light from above, so light may well play a modifying role. At intermediate, nonstress salinities, the animals shifted consistently downward with illumination from above and more strongly downward with illumination from below. No adaptive advantage is postulated here and no marked responses were expected. Perhaps with no salinity stress gravity and light exert antagonistic effects on the animals with illumination above. Thus, the animals might be found in either half of the column. Whereas, with illumination from below, the two cues work together to yield the strong downward shift. Perhaps crowding interferes with the animals' moyement toward the bottom within the narrow tube, thus upon release into the whole cylinder, the downward shift is made. C. Responses to Changes in Salinity with No Light Source In hopes of gaining further insight on the respective roles of light and gravity as directional cues for copepod movements accompanying changes in salinity, a trial was run in darkness. However, without the aid of an infrared system to view the animals in the dark, light had to be introduced to make the counts. Except for darkness, the experiments were conducted as before. However, after 30 minutes in the dark a light from below was turned on (for less than a minute) just to check for any marked tendency for the copepods in the central tubes to be in either upper or lower half of the column. The animals were released and the light turned off. They were checked again, after 2 minutes, with the same light from below. At low salinities the animals were found on the bottom; at high salinities they moved up to the top (Table 3). These results are in accordance with those obtained with the light from above. In addition, the animals moved in the adaptive direction, an important ability if the animals are to respond correctly in the absence of light as in night. IV. Changes in Vertical Distribution with a Sudden Change in Oxygen Concentration under a Constant Directional Light Source Oxygen concentration in these experiments ranged from 1.5ppm to off scale 20"ppm. Low oxygen sea water was made by bubbling with nitrogen; high oxygen water was made by bubbling with oxygen. Oxygen concentrations of the test media were determined, following completion of the 2 minute count, with an oxygen meter (Yellow Springs Instrument Co., Inc. Model 54). The listed values are probably reliable to +.5ppm. Each graduated cylinder was covered with parafilm during the tests to minimize gaseous equilibration with the atmosphere. A. Responses to Changes in Oxygen Concentration with Constant Light from Above. The various trials show some consistent trends (Table 4, fig. 4): 1) At low oxygen concentrations (1.5ppm to 2.5ppm) with illumination from above, the animals shifted strongly up towards the light resulting in almost all of the animals in the top quarter of the column at the 2 minute count. 2) Through the rest of the range, intermediate to high oxygen content, only a slight downward shift occurred, with animals still distributed throughout the water column. Again, the responses appear to be adaptive. At low oxygen concentrations the best direction to swim in search of higher dissolved oxygen is upward, where greater gaseous exchange could occur at the surface. However, at high oxygen concentrations, behavior does not differ from that exhibited in normal conditions. It is unlikely that in nature dissolved oxygen levels would get sufficiently high to be toxic or provide stress to the animals, and therfore one would not expect the animals to show any marked response. These copepods are routinely found in pools with high photosynthetic activity and supersaturated waters (dissolved oxygen = 12ppm - 16ppm). When introduced to low oxygen water the animals were positively phototactic and negatively geotactic. Again, experiments with light from above do not supply information on the respective roles of gravity and light. In the next set of experiments light was offered from below. B. Responses to Changes in Oxygen Concentration with Constant Light from Below With illumination from below, in tests at all oxygen tensions, the animals showed a marked movement downward (Table 5, fig. 4). At the 2 minute count almost all animals were found within the bottom quarter of the column (fig. 4). If gravity were the predominating cue at low oxygen levels no change in distribution from experiments with light from above would be expected, but this result was not obtained. If light were the predominating cue at low oxygen tensions, the animals would be found at the bottom of the column in these tests. The results fall in accordance with this model. Thus, despite the adaptive advantage of going up upon encountering low oxygen concentrations, the animals went down with light from below, suggesting light as the predominating directional cue. As in nonstress salinity changes, upon encountering intermediate and high oxygen tensions, the animals shifted markedly downward with light from below but only slightly dowward with light from above. V. Changes in Vertical Distribution with a Sudden Change in pH under a Constant Directional Light Source pH values ranged from 4.5 to 10.5. Solutions were acidified with IN HCl and made basic with IN NaOH. The precipitate formed upon addition of base was removed by filtration through Whatman No. 1 paper. The pH was determined using a Beckman pH meter. A. Responses to Changes in pH with a Constant Light from Above With light from above, the animals shifted toward the bottom at the pH's differing from normal, 8.4 (Table 6, fig. 5). However, eyen the pH test choices closest to the normal were rather extreme in view of very slight pH fluctuation found in the field (Burnett 1977, pers. comm.). Also Adaptive responses under stressing pH's may not have been selected for as strongly as for other environmental stresses such as salinity or low oxygen concentrations. Furthermore, there is no obvious direction (up or down) to swim to effectively avoid stress-exerting pH conditions. At the altered pH's tested the animals were positively geotactic and negatively phototactic with light from above. B. Responses to Changes in pH with a Constant Light from Below With light from below, animals at all pH's shifted strongly dowward (Table 7, fig. 5). If light were the predominating cue at altered pH's 0 the animals would be found at the top with light from below. However, the animals move to the bottom with light from below as they did under light from above, the result predicted if gravity were the stronger cue. As in salinity and oxygen experiments at normal conditions, the animals shifted slightly downward with light from above and strongly downward with light from below. VI. Summary 1) The short term responses to sudden changes in salinity, oxygen concentration, and pH, in terms of tendency to swim upward or downward, were studied using a light coming either from above or below, to investigate the role of light as a directional cue to vertical moyement. 2) At low salinities, the adaptive response should be to swim down; nommally this means away from the light and toward gravity. Accordingly, with light from above the animals were negatively phototactic and positively geotactic. However, with light from below, most animals swam down toward gravity and fewer animals were found at the top, away from light. This result suggests gravity over light as the predominant directional cue for vertical movement, with light playing a modifying role. 3) At high salinities, the adaptive response should be to swim up; normally this means toward the light and away from gravity. Accordingly. with light from above, the animals were positively phototactic and negatively geotactic. However, with light from below, most animals swam down toward the light, and fewer found on top away from gravity. This result suggests light over gravity as the predominant directional cue for vertical movement at high salinities, with gravity playing a modifying role. 4) The animals are capable of responding in an adaptive manner when confront 2 with a change of salinity in the absence of light, with gravity providing the only directional cue. 5) At low oxygen tensions, the adaptive response should be to swim up; normally this means toward the light and away from gravity. Accordingly, with light from above the animals were positively phototactic and negatively geotactic. However with light from below the animals swam down, again positively phototactic, but in this case positively geotactic. This result suggests light as the predominant cue for vertical moyement at low oxygen concentrations. 6) At pH's other than normal (8.4) the animals shifted in the direction of gravity, with little effect seen with a change in the direction of the light source. 7) In all cases, upon release of the animals into the normal or nonstress conditions tested, they shifted slightly downward with light from above and markedly downward with light from below. 8) In conclusion, reproducible trends to move with or against gravity and towards or away from a directional light source offered from above or below are seen in response to a sudden change in environmental conditions, suggesting the role of both light and gravity in governing directional movement within a vertical column. EFERENCES Dice, L.R. 1914. The Factors Determining Vertical Movement of Daphnia, J. Animal Behavior 4:229-265. Herter, K. 1927. Taxieu und Tropismen der Tiere, Tabulae Biol, 4:348-381. Loeb, J. 1893. Über künstliche Umwandlung positiv heliotropischer Tiere in negativ un umgekehrt, Arch. ges. Physiol. Pflüger's 54:81-107. Loeb, J. 1906. Ueber die Erregung von positiven Heliotropismus durch Säure insbesondere Kohlensäure und von negativen Heliotropismus durch ultraviolette Strahlen. Arch. ges. Physiol. Pflüger's 115:564-581. Rose, M. 1925. Contribution à l’etude de la biologie du plankton, Arch. Zool. expte et gen 64:387-542. Waterman, T.H., The Physiology of Crustacea-Sense Organs, Integration, and Behavior, Academic Press, New York, 1961, v.2. Table I presents the data on changes in vertical distribution with a sudden change in salinity with a constant light source from above. The time of day that each series of tests was carried out is listed with the trial number. The number of animals counted in each of the segments (1-4) of the cylinder at 0' and 2' is listed for each salinity tested. The shaded areas indicate cases in which animals escaped the inner tube prior to the 0' and thus these data points were not included in the composite tables. L 8 16 TABLE 1 TABLE 1 2' 2' 2' 17 ATRIAL 3 2.0 2400 34 PPT 134 34 110 — — TRIAL +2 0100 e 34 54 34 80 34 —— TRIAL +3 13 1700 PPT34 34 60 34 34 34 110 — 2' ATRIAL 3 2 +4 20 0200 134 34 34 PPT 25 A34 34 — 2' 15 70 TOTAL COUNTS 60 134 Pe — — 2 27 45 22 135 33 8 100 34 PPT34 6O 110 34 L 8 46 14 Table 2 presents the data on changes in vertical distribution with a sudden change in salinity with a constant light source from below. The time of day that each series of tests was carried out is listed with the trial number. The number of animals counted in each of the four segments (1-4) of the cylinder at O and 2' is listed for each salinity tested. L I L TABLE 2 2' 1 AERIAL 4 3 12 0300 PPT 34 34 34 — — 2' 0 ITRIAL *2 o 1500 34 PPT 134 — — 2' ATRIAL + +3 0 20 1600 31 25 10 34 PPT 1134 2 6 TOTAL COUNTSE o 16 10 53 122 34 34 34 PPT L 2' 10 516 2 2 % 0 21 30 2 10 4 1337 58 88 31 25 APPT 10 — 60 O 2 31 — 2' O 60 — 60 31 2 1 10 30 85 28 — 31 34 114 2 32 110 Table 3 presents the data on changes in vertical distribution with a sudden change in salinity with no light source. Just prior to releasing the animals the light was turned on just long enough to check for any marked tendency to be in either upper or lower half of the water column. No such distribution was noted. The light was not left on long enough to take a count: consequently, only the 2' counts were obtained. ( Z TRIAL 1800 % TABLE 3 — PPT — 20 10 34 PPT 34 — — 3+ — 2' 20 25 50 — 110 110 7 20 Table 4 presents the data on changes in vertical distribution with a sudden change in oxygen concentration with a constant light source from above. The time of day that each series of tests was carried out is listed with the trial number. The number of animals counted in each of the four segments (1-4) of the cylinder at 0' and 2' is listed for each oxygen concentration tested. TABLE 4 2 — — —L 13 0 — o + — O - + — + 1o + L - —4— 0 + 10 SL 2 —brmhndm 91 immerhme 2 20 &a * X* 3 lsodwoo Aogv IH — Table 5 presents the data on changes in vertical distribution with a sudden change in oxygen concentration with a constant light source from below. The time of day that each series of tests was carried out is listed with the trial number. The number of animals counted in each of the four segments (1-4) of the cylinder at 0' and 2' is listed for each oxygen concentration tested. TABLE — 8 3 i — — -O 0 1 OO S g E4 M9 1H517 o o 0 0 + Sin 9 o — : — + —. N — 2 0 — — iisodwoo — Table 6 presents the data on changes in vertical distribution with a sudden change in pH with a constant light source from above. The time of day that each series of tests was carried out is listed with the trial number. The number of animals counted in each of the four segments (1-4) of the cylinder at 0' and 2' is listed for each pH tested. L O I 11 TABLE 6 ITRIAL 2300 38.4 18.4 TRIAL 42 O130 8.4 p 194 — TRIAL +3 15 1300 8.4 4.5 1e TOTAL COUNTS 117 52 p 8.4 84 — 28 % 1333 87 4 184 0 1484 — 2' 2 6.O 8.4 8.4 9.5 10.5 17 10.5 8.+ 8.4 6.O 3 + 10.5 84 9.5 6.0 8.4 2 2' 11 8 12 35 10.5 9.5 8.4 8.4 18: 2 3 20 58 10.5 6.0 8.4 8.4 9.5 8.4 25 2 Table 7 presents the data on changes in vertical distribution with a sudden change in pH with a constant light source from below. The time of day that each series of tests was carried out is listed with the trial number. The number of animals counted in each of the four segments (1-4) of the cylinder at 0' and 2' is listed for each pH tested. — TRIAL 1500 + TRIAL L 72 1700 TOTAL COUNTS 11 d % TABLE 7 2' 2' 1 3 184 184 6.O 8.4 8.4 — 20 8.4 6.0 18.4 8.4 8 — 11 112 p 8.4 8.1 84 8.4 584 o 5 90 18.4 8.4 p 184 8.4 8.4 9.5 2' 15 10.5 8.“ 8.4 10.5 2' 84 85 10.5 27 Figure 1 diagrams the physical aspects of the experimental set-up. The 50ml graduated cylinder was placed in a constant directional light offered from above or below. Light intensities were measured with a Li-Cor photometer (model LI-185) with the sensors oriented facing the light source and parallel to the axis of the graduated cylinder. Figure 2 diagrams the protocol used in all experiments. 2 Zem LIGHT ANIMALS ENVIRONMENT TIME 0.3 cm — normal sea water 20 females vith egg sat FIGURE 1 + LIGHT SOURCE 0 above or below /1 15 watt fluorescent bulb diam=21cm 30cm distance between light &a water column 120 ux zom Mendemn S photometer sensors u 50m graduated cylinder FIGURE 2 pH 8.4 NORMAL: 34%o 6.5-7.OppmO2. 20-22?c. ZOMIN COUNT ---- 2 2P MIN TEST ARELEASE COUNT 2 — R — 30 0 "igure 3a presents a composite of 4 trials on changes in vertical distribution with a change in salinity with light from above. Each horizontal bar within the outlined shapes represents the percentage of animals tested found in each of the 4 segments (1-4) of the cylinder at 0' (top) and 2' (bottom). Analogously, figure 3b presents a composite of 3 trials with changes in salinity with light from below. L L P N E MSV THO FIGURE 3 e 42 —2 D — s L L L NO 1 MOTT. Figure 4a presents a composite of 3 trials on changes in vertical distribution with a change in oxygen concentration with light from above. Each horizontal bar within the outlined shapes represents the percentage of the animals tested found in each of the 4 segments (1-4) of the cylinder at 0' (top) and 2' (bottom). Analogously, figure 4b presents a composite of 2 trials with changes in oxygen concentra tion with light from below. 39 FIGURE 4 6.5 6.5 . 55 5 b.5 55 5 L PPM 5.5 6.5 8.0 15 25 15.U 11.0 A.U — CT as — L aaaakaa ai e e et ei e e e i se. PPN 6.5 6.5 6.5 6.5 6.5 5.5 6.5 a b. L a . en 110 80 204 srern 0 Figure 5a presents a composite of 3 trials on changes in vertical distribution with a change in pH with light from above. Each horizontal bar within the outlined shapes represents the percentage of the animals tested that were found in each of the 4 segments (1-4) of the cylinder at 0' (top) and 2' (bottom). Analogously, igure 5b presents a composite of 2 trials with changes in pH with light from below. 4 FIGURE 5 L L J D L L o I P L Erie D L J a — L — — MORa THST 36