A tidal rhythm in P. crassipes M. Holdren, D. Sandberg 1 INTRODUCTION The lined shore crab, Pachygrapsus crassipes Randall, inhabits the rocky intertidal region of the western coast of North America. Generally it is found from the zone of lower tides up to the high splash zone in areas where there are pools, crevices, and boulders. P. crassipes may be found higher and lower if vertical crevices are present and it is able to migrate up and down with incoming and receding tides. They are also found in tide pools of varying depths. Crevices offer protection from wave action and from predators as well as providing a damp surface to prevent the crab from desiccating. Close associations with tide pools aid the crab in this respect (Hiatt,1948). Previous studies on P. crassipes include the major work on its biology and molting cycle (Hiatt,1948), osmotic regulation (Gross,1955,1957,1958; Prosser et al.,1955), and reproduction (Boolootian,1965; Bovbjerg,1960a). Virtually no previous work has been done with regard to rhythmic activity patterns. Studies conducted by Hiatt indicated P. crassipes was primarily active during the hours of dark¬ ness. This observation was also reported by Bovbjerg (1960b) and Knudsen (1964). Endogenous rhythms have been discovered in other crabs. An endogenous tidal rhythm has been discovered in a fiddler crab by Palmer (1975). He found the rhythm could persist in the laboratory for up to 5 weeks, but was most often damped out rather quickly. The fiddler crab was most active at low tide. A tidal rhythm in P. crassipes M.Holdren, D.Sandberg In preliminary studies done during the month of April 1978 few crabs were seen at night, contradicting the observations of Hiatt, Bovbjerg, and Knudsen. This contradiction and the question of whether P. crassipes displays an activity rhythm comprise the focus of this investigation. MATERIALS AND METHODS Field Studies Field studies on P. crassipes were carried out at Mussel Point, Pacific Grove, California between 26 April and 3 May 1978. One area observed was between the +2 and 8 ft. tide level and measured 7x8 meters. It was massive granite containing large horizontal and vertical rock surfaces, crevices, and part of a large pool, into which seawater would flow with incoming tides. A lower intertidal observation area was from the -1 to +3 ft. tide level, and measured 5x5 meters. Observations were made by sitting on top of a tall boulder and remaining relatively still. The crabs did not seem to notice the observer during the day unless the observer moved close to the crab or shadows passed near the crab. During the day observations were made from above with a pair of Bushnell Sportview 7x35 binoculars. At night observations were made using a Barsom infrared viewer. The area was continuously monitored over a 48 hour period during the study. At 8 hr. intervals weather con¬ ditions, the temperature of rock surfaces and crevices were recorded. Whenever a crab was sighted notes were made of A tidal rhythm in P. crassipes M.Holdren, D.Sandberg (1) the time (2) the height in the intertidal where the crab was seen (3) the type of surface it was on, i.e. rock, crevice, or pool (4) if the surface was wet or dry, and (5) if the crab's activity was solitary or social. If the crab was moving, the direction of movement, either toward or away from the action of the waves, was recorded. Brief observations of the area were made during the nights of 2 May and 3 May 1978, when lower low water occurred shortly after midnight. These observations were made with the infra¬ red viewer. Activity Wheel Experiments Six crabs with carapaces measuring 1.5-2.5 cm. across were captured and each placed into activity wheels (Figure 1). The activity wheels, made of plexiglass, revolve freely about a stationary rod. Complete revolutions of each wheel were recorded as deflections using an Esterline Angus strip chart recorder. Each wheel containing a crab was placed in a part¬ ition of a light tight box. Running seawater was kept at a level to just cover the lower edge of the revolving wheel(Fig. 2). Food was provided in the form of Macrocystis pyrifera, attached in a bundle to the side of the cage. This procedure was used in experiments with three light regimes: LD 12:12, DD, and LL. The light source was a flourescent tube which provided a light intensity of 2.4 pE/m/sec at a distance of 1 ft. In experiments where activity was very high, (LD), data from the recorder was scored on a scale of O to 5, with O indicating no activity during a one hour period and 5 indicating A tidal rhythm in P. crassipes M.Holdren, D.Sandberg continuous activity throughout the hour. The activity of each crab was scored for every hour of the study. The data were normalized as hourly percentages of total activity which were then summed and plotted as mean values for all experimental animals. In activity wheel experiments in DD and LL, activity was plotted as summed hourly deflections for each individual. These values were normalized as hourly percentages of total activity to get a grouped plot for the DD study. Differences between activity at rising and falling tides and differences in activity at high and low tides were calculated using a Chi-square test. Simulated Natural Environment In addition to field observations and recordings of individuals in activity wheels, observations were also made on groups of crabs in captivity. A large fiberglass tub (Fig. 3), approximately 1 me, located out of doors was used for these studies. Intertidal rocks were arranged in the tub to simulate the natural environment. A few mm of sea water flowed across the bottom and algae was present for food. A Panasonic dim light TV camera was positioned four to five ft above the center of the tub to view the entire surface. Activity was recorded on video cassettes for five minutes every hour, and viewed on a Panasonic closed circuit TV monitor. Each observation was scored for the number of crabs that were visible. A crab was defined as "active" if it could be seen and positively identified as a crab, either by its shape or by movement. In other words, it had to be out in the open. A tidal rhythm in P. crassipes M.Holdren,D.Sandberg or, if partly obscured, it had to move about in order to be considered active. Nearly all crabs counted did move around during the sample periods. Natural Light Cycle For the first set of observations using the set-up described above, fifteen crabs, measuring about 3 cm across the carapace, were collected and placed in the tub the day before observations began. The population density in the tub did not exceed densities that can be found in the field. The light conditions under which the observations were made were sunlight during the day and a 25 watt incandescent bulb with a red plastic filter at night. The light intensity was low; the minimum required by the sensitive dim light camera to resolve the crabs and would not register on a meter sensitive to 1 ft candle. But in order to control for possible effects of the red light on the crabs, an infra¬ red viewer was used for part of one night to count the crabs. This device allows the user to see objects illuminated with infrared radiation and requires no visible light. The numbers of crabs seen this way did not differ noticeably from those obtained with visible red light. This is in agreement with Hiatt's claim that artificial illumination does not disturb their foraging habits. Dim Light It was also of interest to see how a group of crabs would respond to a situation where the light intensity did not change from day to night. Such a situation would A tidal rhythm in P. crassipe M.Holdren,D.Sandberg be free of one type of external information about time of day. The same materials and methods as before were used for the second set of observations, except that the tub was covered with two layers of 3 mil black plastic. This covering was entirely opaque to visible sunlight. However, it was found that a very faint glow of light did get through the fiberglass sides of the tub during the day. Therefore, a completely constant light condition was not achieved. The red lamp illuminated the tub the entire time. RESULTS Field Studies Activity during the 48 hr study peaked around lower low water between the hours of 0800 and 0900. A second peak was observed on the second day shortly after sunset, as noted by Hiatt (1948). During periods of high activity (Fig. 4) the majority of crabs were seen either feeding on or moving across dry, exposed rocks. As the tide rose the animals moved away from the action of the waves, into crevices. Although very few social interactions were noticed, those observed usually lasted only a few seconds. Crabs seen in crevices were usually wedged in motionless. Often a bubbling sound could be heard coming from the crabs in crevices. On several occasions individual crabs were seen covering themselves with froth. No reference to either behavior could be found. Crabs were observed on lower rocks at lower low water during the nights of 2 May and 3 May 1978. The number seen A tidal rhythm in P. crassipes M.Holdren,D. Sandberg at night during lower low water was comparable to the number observed at lower low water during the day, although no quantitative information was recorded. LD 12:12 - Activity Wheel A plot of mean percent activity versus time shows that more activity occurs during the daylight hours (Fig. 5). A Chi-square test comparing activity in light and dark shows that there is significantly more activity in light than in dark (.Olpg.025). Peaks of activity occur during hours of darkness. The means of these activity peaks, excluding activity in light, were calculated by averaging the percent activity over three or four hours to either side of the hour of greatest activity. A least squares linear regression on the relationship between the means and corresponding days, shows a slope of .87. Multiplied by 60 minutes, this slope represents a daily phase advance of 51.9 min. The correlation coefficient for this linear regression is.92 (Sokal and Rohlf, 1969). DD - Activity Wheel Two of the 3 crabs recorded in DD show significantly more activity during rising tides when analyzed individually. There was no definitive pattern in the activity of the three crabs with respect to low or high tides, i.e. one crab was more active at high tide, another was more active at low tide, and there was no significant difference between activity at high and low tides for another crab. When the data for the crabs were grouped, a substantial peak of activity occurs at hours between low and high tide A tidal rhythm in P. crassipes M.Holdren, D.Sandberg between the hours of 1400 and 2400 (Fig. 6). The slope of the regression line for these peaks is .94, representing a phase advance of 56.6 minutes per day. The correlation coefficient is.86. LL - Activity Wheel Statistical analysis of activity wheel recordings of crabs in LL showed conflicting results. Again, data on only three individuals was obtained due to equipment failure. Though one crab showed more activity at rising tides than at other times, another showed perfectly random activity with regard to tides when subjected to a Chi-square test. The third one turned the wheel almost incessantly and at what appeared to be the same pace for many hours. Simulated Natural Environment - LD When the absolute numbers of crabs counted as active each hour are graphed versus time, a repeating pattern appears (Fig. 7). Very noticeable peaks of activity coin¬ cide with the hours around lower low water which occurs just before noon on these days. Fewer crabs are active at other times, particularly at night. Simulated Natural Environment - Dim LL Similarly, the graphed results of observations on crabs in continuous dim light show peaks of activity at lower low water during the day (Fig. 8). Note also the major burst of activity that occurs on the second night at hours corre¬ sponding to low tide. This double peak occurs at the semi¬ lunar shift of lower low tides. There were not enough cycles for analysis of phase shift. A tidal rhythm in P. crassipes M.Holdren,D.Sandberg DISCUSSION Early in our studies on activity patterns in Pachy- grapsus crassipes field observations showed a peak of activity at lower low water both during the day and at night. This is in conflict with previous reports which indicate activity during the hours of darkness (Hiatt, 1948; Bovbjerg, 1960b; Knudsen, 1964). Since these studies indicated a tidal rhythm of activity in field conditions we began studies in the laboratory away from tidal influence and under a variety of light regimes to investigate activity patterns and their possible endogenous nature. A 24 hour light-dark cycle is known to keep a tidal locomotion rhythm at a strict tidal frequency, though under constant conditions there is an average free running period of 24 hr 55 min (Enright, 1972), which is a phase advance of the tidal period of 24 hr 51 min. The presence of a tidal rhythm in P. crassipes is supported by analysis in LD 12:12 where peaks occur with rising tide during the hours of darkness. Analysis of the means of the activity peaks shows a phase advance of .9 min per lunar day. P. crassipes appears to maintain a strict tidal rhythm in LD 12:12. Analysis of activity peaks during rising tides in DD during the subjective night shows a free running period of 24 hr 56.5 min. This may indicate a circalunadian period with a phase advance under constant dark conditions. However, the sample size and period of the experiments is A tidal rhythm in P. crassipes M.Holdren,D.Sandberg insufficient to establish this with certainty. Further evidence to support the hypothesis of a tidal rhythm comes from the study in the outdoor tub in constant dim light. On the second day of the study low low water and high low water were about equal in magnitude and shifted positions from day to night. The crabs showed peaks of activity at both of these low tides, apparently following the tidal shifts. This suggests that the crabs' activity rhythm anticipated the semilunar shift of low tides. This result certainly deserves further investigation. A small peak of activity was observed in the field shortly after sunset on the second day of the 48 hour study. No data were available for the first day during this time. Activity after sunset was also reported by Hiatt (1948). Therefore, both tidal factors and the natural light-dark cycle may affect activity. A circadian activity rhythm in the crabs was not conclusively shown by these data, but the possibility of one can not be ruled out. Crabs kept in activity wheels on a LD 12:12 regime displayed greater activity when the light was on. The environment was artificial in that the crabs did not have crevices for hiding places. The reason for activity in the light is open to speculation. The running could be an escape response. When exposed to constant light, the crab's behavior was erratic. Since no two crabs exhibited the same behavior, no conclusions can be drawn. 10 A tidal rhythm in P. crassipes M.Holdren,D.Sandberg Though field data are indispendible for an understanding of Pachygrapsus crassipes behavioral patterns, these crabs are so alert and cryptic that rigorous descriptions of their movements in the field are difficult to obtain. The two most successful methods in these studies were recording from activity wheels and viewing small groups of crabs in semi-natural aquaria. These results suggest that P. crassipes has an endogenous activity rhythm phased to the tides. Further studies are necessary to determine the relationship between circatidal and circadian variations in activity in the observed rhythm in Pachygrapsus crassipes behavior. SUMMARY 1. Studies in the field and in the laboratory removed from tidal fluctations indicate a tidal rhythm of activity in P. crassipes. The crabs are most active at lower low water. The phase advance in LD 12:12 was found to be .9 min per lunar day. In DD the phase advance was found to be 5.5 min per lunar day. When the times of lower low water shifted from day to night, crabs showed peaks of activity at both low tides. This suggests that the crabs' activity rhythm follows lower low water through the semi-lunar shifts of low tides. A circadian rhythm was not found in this investigation. However, activity after sunset and the effect of light on the activity patterns of crabs in running wheels A tidal rhythm in P. crassipes M.Holdren,D.Sandberg 12 suggest that light plays an important role in modifying the crabs' behavior. A tidal rhythm in Joldren, D.Sandberg 13 ACKNOWLEDGEMENTS We would like to thank our advisor, Chuck Baxter, for encouragement at every stage of our study and for preparing us well for our oral presentation. We are indebted to Dr.Robin Burnett for assistance in many aspects of this study, and Lawrence W. Harding, Jr. for careful reading of this paper, many helpful suggestions, and coffee. We appreciate our fellow students who were our ever-present supportive companions as one 24.8 hour day led to the next. A tidal rhythm in P. crassipes M.Holdren,D.Sandberg LITERATURE CITED Boolootian, R.A. 1965. Aspects of reproductive biology in the striped shore crab Pachygrapsus crassipes. Bull. So. Calif. Acad. Sci. 64:43-44. Bovbjerg, R.V. 1960a. Courtship behavior of the lined shore crab, Pachygrapsus crassipes Randall. Pacif. Sci. 14:421-422. Bovbjerg, R.V. 1960b. Behavioral ecology of the crab,Pachy¬ grapsus crassipes. Ecology 41:668-672. Enright, J.T. 1972. A virtuoso isopod: Circa-lunar rhythms and their tidal fine structure. J. Comp. Physiol. 77:141-162. Gross, W.J. 1955. Aspects of osmotic regulation in crabs showing the terrestrial habitat. Amer. Natur. 89:205-222. Gross, W.J. 1957. A behavioral mechanism for osmotic regulation in a semi-terrestrial crab. Biol.Bull. 113:268-274. Gross, W.J. 1958. Potassium and sodium regulation in an intertidal crab. Biol. Bull. 114:343-347. Hiatt, R.W. 1948. The biology of the lined shore crab, Pachygrapsus crassipes Randall. Pacif. Sci. 2:135-213. Knudsen, J.W. 1964. Observations of the reproductive cycles and common Brachyura and crablike Anomura of Puget Sound, Washington. Pacif. Sci. 18:3-33. Palmer, John D. 1973. Tidal Rhythms: The clock control of rhythmic physiology of marine organisms. Biol. Rev. 48:377-418. 14 A tidal rhythm in P. crassipes M.Holdren, D.Sandberg Palmer, John D. 1975. Biological clocks of the tidal zone. Sci. Amer. 232(2):70-79. Prosser, C.L., J.W. Green, and T.J. Chow, 1955. Ionic and osmotic concentrations in blood and urine of Pachygrapsus crassipes acclimated to different salinities. Biol. Bull. 109:99-107. Sokal, Robert R. and F. James Rohlf. 1969. Regression, pp.424-425. Biometry, W.H. Freeman and Co., San Francisco.776 pages. A tidal rhythm in P. crassipes M. Holdren, D. Sandberg Figure 1. Activity wheel with revolving cage, magnet, and switch. — A tidal rhythm in P. crassipes M.Holdren,D.Sandbei Figure 2. Activity wheels set up in light¬ tight box and supplied with running seawater. 18 A tidal rhythm in P. crassipes M.Holdren, D. Sandberg Figure 3. Schematic diagram of the outdoor tub as seen on the TV monitor used for observations. The relative sizes of the rocks and a crab in relation to a 1 m tub are depicted. 5 S A tidal rhythm in P. crassipes M.Holdren,D.Sandberg Figure 4. Total numbers of crabs observed at half-hour intervals in field studies. The position of the tide and the day/night cycle are indicated. saai . *............ . aaaaaaa- + a- - . t . . . a- aaaaa- : :... a + ... . - - * . . SSVäO 20 HZSMON A tidal rhythm in P. crassipes M.Holdren,D.Sandberg The average percent of total activity Figure 5. of 4 crabs for 7 consecutive days from 6 to 12 May, 1978. These studies were conducted in LD 12:12 Subjective tidal conditions and the imposed light¬ dark cycle are indicated. The black line represents a least squares linear regression fit to the means of the night activity peaks. 215 10 157 04 08 12 46 20 0 TIME M.Holdren,D.Sandberg A tidal rhythm in P. crassipes Average percent of total activity for Figure 6. 3 crabs in activity wheels in DD for 6 consecutive days from 18 to 23 May, 1978. Subjective tidal conditions and the light-dark cycle are indicated. The black line represents a least squares linear regression fit to the means of the activity peaks occurring between 1600and 2000. 10- 20 5. 2.0 5 10 . . . . . . . . . . . . . . . . 04 da 16 20 00 72 TIME e A tidal rhythm in P. crassipes M.Holdren,D.Sandberg Figure 7. Number of crabs observed active (n=15) in the outdoor tub under natural light¬ dark conditions. NUMBER OF CRABS . . . s . . - a. . . . . TIDES L . e A tidal rhythm in P. crassipes M.Holdren,D.Sandberg Figure 8. Number of crabs observed active (n=15) in the outdoor tub under constant dim light. . e*- . - . - - . NUMBER OF CRABS . . . . . TIDES