Rhythmicity under constant conditions in the rock crab, Cancer ...

BULLETIN OF MARINE SCIENCE, 36(3): 454-466,1985

RHYTHMICITY UNDER CONSTANT CONDITIONS IN THE ROCK CRAB, CANCER IRRORATUS Steve Rebach ABSTRACT The existence of activity rhythms in migratory populations of the rock crab, Cancer irroratus, which spend most of the year in deep water, was investigated. Mature individuals from the Mid-Atlantic Bight were tested under laboratory conditions of constant light (LL) and constant dark (DD) after an initial ambient photoperiod was presented. Activity levels were simultaneously monitored for 20 crabs maintained in separate compartments, using an infrared beam-break system. Activity was analyzed using an Enright periodogram. Activity under LL was at a relatively low level and with no rhythmic periodicity exhibited. In DD, activity was concentrated at approximately 25-h intervals, approximating a tidal period. Under ambient (natural photoperiod) conditions, a 24-h rhythm was present with activity greatest during the scotophase and with peaks at dawn and dusk. Possible advantages to the presence of a tidal rhythmicity in a deep water species are discussed and include temporal partitioning of the environment, a timekeeping mechanism for the initiation of migration, and an evolutionary or ecological remnant from shallow water populations.

The common rock crab, Cancer irroratus, is found from Labrador to South Carolina (Haefner, 1976) and is most abundant from Maine to North Carolina. Rock crabs inhabit cold water (5 -15°C, Haefner, 1976) and in the mid-Atlantic region they live at depths of 10-700 m (depending on age and season), with highest densities between 40 and 60 m (15-30 km offshore) (Musick and McEachran, 1972; Haefner, 1976). Rock crabs in this region also undergo a yearly mass migration into inshore and lower Chesapeake Bay areas (depths of 1-20 m) in October/November and remain until March/April (Shotton, 1973; Haefner and van Engel, 1975). Since some rock crabs enter Chesapeake Bay, they can tolerate some degree of fresh water, but they do not survive in salinities lower than 200/00 (Haefner and van Engel, 1975). Molting occurs in this region from December to February (Winget et al., 1974), with females undergoing their yearly molt in December (Terretta, 1973) in preparation for mating. Molting and mating are confined to the shallower areas of the continental shelf. After mating occurs, the female returns to offshore waters. The males remain along the shelf, or move to even shallower areas, molting in January and continuing to feed in shallow water until spring (Terretta, 1973). A review of this migration can be found in Rebach (1983) and a synopsis of biological data on Cancer irroratus in Bigford (1979). Green crabs, Carcinus maenas, exhibit two rhythms, circa tidal and circadian, in which peaks of activity occur at high tide, with the greatest activity during a nighttime high tide. Over time, the smaller daytime peak increases as it approaches midnight and the larger nighttime peak decreases as it approaches dawn. Under constant conditions, the tidal rhythm persists for about a week. Crabs kept in the laboratory for a month showed a circadian rhythm with no tidal component (Naylor, 1958; 1962). Sand fiddler crabs (Uca pugilator) exhibit an activity pattern with directionality dependent on the stage ofthe tide (Hermkind, 1968; 1972). These directionalities can be exhibited in the laboratory, far removed from the beach. Brown et al. (1956) and Bennett et al. (1957) observed a spontaneous tidal locomotor rhythm in Uca pugnax. Statistical manipulation of the data uncovered 0

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an underlying, lower amplitude, diurnal rhythm (although some controversy still exists on this point-for a review of this aspect see DeCoursey, 1983). Other physiological systems in this genus exhibit circadian and tidal periodicities. Color change (melanophore activity) (Brown and Webb, 1948) and oxygen consumption (Brown et al., 1954) are but two well known examples. Evidence indicates a relationship between solar and lunar rhythms in Uca (Barnwell, 1966; Brown et al., 1953; Webb and Brown, 1965). Reviews of movements and rhythmicity in Uca and in Carcinus can be found in Palmer (1974), Creutzberg (1975), Rebach (1983) and Webb (1983), and of Uca in Hermkind (1972). Many workers have found both solar and tidal components in other intertidal species of crabs. For a review of these rhythms and the relationships between solar and tidal periodicities see Palmer (1974; 1976), Aschoff (1981), DeCoursey (1983) and Webb (1983). The rock crab, Cancer irroratus, spends 5 to 7 months each year offshore in deep waters, where photoperiodic cues are not readily available, and the remainder of its time in shallow coastal waters where it comes under the influence of both solar and tidal periodicities. Furthermore, populations ofthis same species appear to be non-migratory in New England (Turner, 1953; Saila and Pratt, 1973), where they spend the entire year in shallow water. In this study, animals from midAtlantic populations were tested for rhythmicity (as evidenced by locomotor activity). Terrestrial animals (including semi-terrestrial Crustacea) utilize circadian entraining agents such as photoperiod and, to a lesser extent, temperature cycles. Intertidal crustaceans usually do not respond strongly to light-dark cycles and entrain to artificial tides, simulated wave action, and cycles of temperature and/or salinity changes associated with tide (DeCoursey, 1983). This population was chosen because of its seasonal change of habitat (from deep to shallow waters) and the accompanying difference in available cues to which it is exposed. METHODS AND MATERIALS Rock crabs were captured at different times of year by bottom dredge from the New York Bight to the Mid-Atlantic Bight at depths that ranged between 20 and 70 m. The mean depth of capture was 23 m. Most samples produced an approximate I: I ratio of males to females. Some samples, especially those taken during the migratory period, resulted in ratios as high as 16: I male: female. The mean (±I SO) point-to-point width was 59.6 ± 14.4 mm. The mean weight (±l SO) was 39.9 ± 29.1 g, and the overall sex ratio was 1.8: I m:f. Gonadal inspection of males and the presence of eggs on females from the coastal areas near Virginia suggested that southern populations may mature at about 30 mm carapace width (Shotton, 1973). The size at sexual maturity is greater in the northern part of their range (60 mm, Scarratt and Lowe, 1972). AIl animals tested were sexually mature (confirmed by post-mortems). After capture, crabs were transported to the laboratory within 1-3 h in chilled, light-tight containers. They were maintained in combined housing and testing facilities consisting of duplicate 1,265-liter recirculating, temperature-controlled units, each capable of separately testing 10 crabs (each in an individual compartment) (Rebach, 1977). The two systems were maintained at the same conditions of temperature, salinity, and photoperiod. All activity testing series were conducted simultaneously on 20 crabs. Collection of data from individuals maintained in separate compartments, but under identical conditions (since each set of 10 shared a common water supply), permitted treatment as replicates. Many earlier studies used "actographs" of various designs for measuring locomotor activity. Most of these involved tipping containers, pie plates or buckets to make an electrical contact. These containers were usually very small and locomotor activity was severely restricted. The compartments (26 x 48 cm each) used in this study did not restrict movements and allowed recordings of natural activity patterns. Activity was measured by infrared beam-break using seven photoresistors (Clairex CL703L-peak sensitivity at 735 nm) wired in series and arranged in an "H" pattern under each of the 20 testing chambers. Four photoresistors were located at the comers of the compartment and three were placed across the center. An integrated circuit a,nplification system was slightly modified from Rebach (1977) to interface with a Hewlett-Packard HP-9815A desk calculator via an HP-98133A BCD interface.

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The calculator produced an hourly printout oftotal activity for each of the 20 test animals. An EsterlineAngus A620X 20-pen continuous event recorder was used as a backup, Between tests, each testing unit was cleaned, water quality analyzed, and 10% of the water replaced with freshly mixed artificial seawater. The crabs were fed daily on a randomized schedule with Crustacean Ration (Rebach, 1981). By using a combination ofrelays and elapsed time meters (Kessler-Ellis Products- ETMVS 15,13) connected to a dimmer switch and a reversible motor, a 20-min dawn was introduced before the photophase ("day") and a 20-min dusk before scotophase ("night") in photoperiod tests, Kavanau (1962) criticized the use of abrupt experimental transitions and demonstrated that LD cycles involving simulated twilight periods permitted a greater degree of experimental control. The times of onset and offset of dawn, day, dusk and night were recorded by the HP-98 I SA. At lights on, light intensity in the tanks was 250-300 lux (approximate light intensity at 10 m), depending on water clarity and turbulence. Pilot experiments conducted over a period of 9 months with a single group of animals held under ambient photoperiod indicated that when rhythmicity was exhibited, the peak became obvious after 1 week, reached its maximum definition during the second week and only began to decrease in amplitude after 6 months of testing. The length of the period (periodicity) was fairly constant. It was, therefore, decided to terminate activity tests as soon as possible after the rhythm was clearly defined (14 days). Some species do not continue to maintain their activity levels for such extended periods. Bregazzi and Naylor (1972) found that activity decreased after 2 weeks of testing in Ta/ilrus sa/talor. Each test presented the crabs with a different LD regime. To determine if circadian periodicity was present, an ambient 11.5: 12.5 photoperiod was presented to the 20 crabs. When rhythmicity was exhibited, the next series used a 14-day period of constant light (LL), followed by a similar period of constant dark (DO). Both tests of constant conditions were repeated 6 months later using different groups of 20 crabs immediately after their capture. Data were analyzed for periodicity by constructing periodograms described by Enright (1965) for each test. Computations were made for periods from 12.0 to 36.0 h in increments of 0.2 h. Figures 1-5 present data from 18.0-36.0 h, the range of periodicities that included a major peak. The amplitude (Ap) is a dimensionless value representing the component of activity occurring at the period indicated. The maximum component of activity for each group of 20 crabs centered around a value which was considered to indicate the periodicity of that group. These data are presented in the top half of each figure. The bottom half of each figure presents the mean hourly activity (MHA) (amount of activity for each hour averaged over the 2-week testing period), indicating the photoperiod presented and including light, dark and twilight periods). This allows examination of actual times of high and low activity. RESULTS

Periodogram analysis of the activity of 20 crabs maintained in constant light (LL) for a 2-week period did not indicate any noticeable concentration of activity (Fig. IA). Activity during the day (MHA) was at a relatively constant and low level (Fig. IB). Replicates conducted at later times, using other groups of crabs, produced similar results (Fig. 2). However, under conditions of constant darkness (DO), a concentration of activity was observed at approximately 25-h intervals (Figs. 3A, 4A). The MHA for the DO tests did not indicate a partitioning of daily activity (Figs. 3B, 4B). However, when this was reconstructed to represent a 25-h day (Figs. 3C, 4C), partitioning was more clearly observed. These data can be compared to the 24-h periodicity typically exhibited by crabs exposed to artificial illumination in phase with, and of the same duration as, ambient photoperiod (Fig. 5A). In this case, locomotor activity is present at a much higher level and greatest during the scotophase (Fig. 5B). Activity is relatively insignificant during the photophase but there are peaks at dawn and dusk. The activity rhythm conforms to the photoperiod presented, and a 24-h periodicity is exhibited. DISCUSSION

In the two series of tests in constant dark, a periodicity close to 25 h, approximating a tidal period, was observed. There was no activity peak in the single

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tidal period of 12.4 h. Periodicity of 12.4 h was also absent in other animals exhibiting tidal (24.8 h) rhythmicity such as isopods (Neumann, 1981) and decapods (Decoursey, 1983). No periodicity was observed in tests in constant light. Earlier work (Fig. 5 and Rebach, 1977) showed that rock crabs offered an ambient, 24-h photoperiod demonstrated a 24-h solar rhythmicity and nocturnal activity. This has also been observed in other studies on Cancer (Fogarty, 1976) as well as in other groups of Crustacea. Although capable of using both a time-compensated sun-compass and a time-compensated lunar compass in its movements on tidal beaches, the sand flea Talitrus saltator is a nocturnal animal whose activity


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is almost entirely suppressed in constant light, and which exhibits no evidence of tidal rhythmicity in activity testing under various photoperiods (Bregazzi and Naylor, 1972). In this study, locomotor activity exhibited peaks related to the twilight periods of dusk and dawn (Fig. 5). Barnwell (1966) also observed an enhancement of tide-related activity in Uca minax for the first few hours after sunrise and sunset. Naylor (1960) showed that the tidal rhythm of Carcinus from a tidal habitat could be suppressed by maintaining the crabs in a non-tidal aquarium for 4 weeks. Their activity then resembled that of crabs from a non-tidal area (a daily rhythm, which also included peaks after dusk and just before dawn). In this study, the crabs were maintained in a non-tidal aquarium but still exhibited a tidal rhythm

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B. Sporadic, non-rhythmic activity under constant darkness with MHA calculated for a 24-h day. C. MHA recalculated for a 25-h day indicating apparent temporal partitioning of tidal day. All notations as in Figure 1.

when placed in DD after 2 months (Fig. 3A) or 3 months (Fig. 4A) of presentation of photoperiods. It is possible that the 25-h periodicity observed in these experiments is not tidal but is an expression of the free-running period of a circadian rhythm under constant conditions. However, under constant conditions, Aschoff's Rule predicts that the free-running period under DD is commonly less than 24 h in nocturnal species (Pittendrigh, 1981) and greater than 24 h in LL. Furthermore, the periodicity for nocturnal animals in LL should be greater than the period in DD (Sollberger, 1965). The rock crab clearly appears to be nocturnal (Fig. 5) but does not exhibit any periodicity in LL, and the period in DD is not less than 24 h. Aschoff (1960) generalizes that environmental factors which cause an increase in activity in a given organism also cause a shortening of the period of the rhythm. This has been demonstrated for the shore crab Carcinus (Naylor, 1963). Therefore, DD, since the crabs are dark-active, should produce a period less than 24 h. Harker (1958) and Naylor (1960) found that rhythms become less precise if

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Figure 4. Activity of another 20 rock crabs tested under constant darkness 6 months later, indicating tidal periodicity (A), lack of ryhthmicity in the MHA when calculated on the basis of a 24-h day (B) and temporal partitioning of the tidal day when MHA is recalculated for a 25-h day (C). All notations as in Figure I.

animals are held in constant conditions, and Neumann (1981) has observed that circatidal rhythms lack the persistence and degree of precision apparent in many circadian rhythms. Decoursey (1983) states that crustacean locomotor rhythms are very noisy and that precision measurement is very difficult even with periodograms. This evidence would indicate that the repeatable, fairly precise, 25-h period observed is not the free-running period in rock crabs. It is possible that free-running periods are not exhibited in animals that respond to two different, strong, exogenous cues such as photoperiod and tide. DeCoursey (1983) states that endogenous timing mechanisms are useful in niches with noisy environmental signals, a situation that is probably not true in the deep water habitat. It is also possible that some organisms do not possess a timing mechanism that is self-sustaining in constant conditions since they rarely find themselves in such environments. Similar experiments with Uca crenulata (Honegger, 1976) indicated that evidence for a free-running period in this species was not particularly convincing.

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20 rock crabs under an ambient photoperiod of day-night cycle. Nocturnal activity (rhythmicity), is exhibited. Solid bar indicates darkness, clear All notations as in Figure 1.

Tidal rhythms are present and adaptive in crabs such as Carcinus maenas that live just below the tide line and Uca spp. that live just above it. They time their movements, activity, courtship, aggression and other aspects of their life cycle to the dominant influence in their lives. However, when these crabs forage at the appropriate cycle of tide, they are vulnerable to many avian and mammalian predators and are, therefore, most active during the nightly high or low tide. This indicates the superimposition of a circadian rhythm on the tidal cycle. On the other hand, Palmer (1971) indicates only circadian components to the activity of four species of "terrestrial" crabs, again influenced by the dominant timing cycle of their environment.

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In the rock crab's deep water habitat, light is not a readily available cue. Measurements at temperate latitudes indicate that the depth for 1% surface light is 16 m in the Woods Hole region (Clarke, 1954; 1969) and 20 m in clear coastal waters, decreasing greatly in turbid areas (Jerlov, 1976). It is not known whether animals living in deeper waters exhibit activity rhythms, and what adaptive benefits might be obtained from these rhythms. The type of rhythm that might be manifested and the cues involved in entraining it have not been studied. When the rock crabs were placed in a situation of constant dark, an activity rhythm was present, although the activity levels were fairly low compared to the levels exhibited in an LD regime, and that activity rhythm was tidal. Fogarty (1976) briefly examined activity rhythms in C. irroratus and the closely related northern rock crab or Jonah crab, Cancer borealis. In the mid-Atlantic region C. borealis are found on the shelfbreak and do not migrate inshore (Haefner, 1977). In New England, where Fogarty did his work, both are found inshore. Fifteen crabs of each species were tested for 5 days each and were presented with the then ambient photoperiod of 14: 10 (no twilight). Data were also analyzed using Enright's periodogram. Both species were nocturnal and indicated a 24-h periodicity (although some variation was found). C. borealis was inactive during the photophase, while C. irroratus' activity was not completely suppressed in the daylight. Although no twilight interval was presented to the crabs, C. irroratus had an activity peak after the onset of darkness and a minor peak after the onset of light. C. borealis only exhibited a peak after the lights were turned off. Fogarty did not report any results obtained under constant conditions such as the constant dark of their deep water habitat. This may even be another example of the suppression of a tidal rhythm caused by maintaining the crabs in non-tidal aquaria as observed by Naylor (1960). Since the present experiments were conducted in recirculating testing facilities in a closed, light-tight laboratory, the cues eliciting tidal periodicity are not clear. Changes in hydrostatic pressure and in temperature caused by the rise and fall of the tide were not present, nor were tidal turbulence and vibration. Only the gravitational changes associated with the moon's passage were present, although it is not known whether many species are capable of detecting these subtle changes. However, Brown (1954) found that oysters transposed from New Haven, CT to Evanston, Illinois opened their shells most at the time of high tide in Connecticut for the first 2 weeks. During the next 2 weeks this gradually shifted to the times of the upper and lower transit of the moon in Evanston. Tidal cues are present at the depths from which the test animals were obtained. Internal waves (Apel et al., 1975) and tidal currents with 2-7 em/sec velocity in the longshore direction (Battisti and Clarke, 1982) with measurable strength in the lunar diurnal period (24.8 h) have been observed at these depths. Tidal periodicities would obviously be most adaptive in environments with pronounced tidal fluctuations. The manifestation of the strongly directed tidal movements found in Uca pugilator (Herrnkind, 1972) depended on the environment inhabited. Herrnkind found that the regularity of the shoreline and the stage of the tidal cycle were important. Responses of crabs from relatively straight beaches were strong and clear. Crabs from shores bordering sinuous tidal canals showed greater dispersion, while those from tidal swamps responded randomly. Naylor (1961) studied Mediterranean Carcinus maenas (since reclassified as C. mediterraneus) from the Gulf of Naples, which has a very small tidal range (0.3 m), and found only a circadian rhythm, as compared to the pronounced tidal rhythms exhibited by individuals from regions where the tidal range was greater (4.3 m).

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One can only speculate as to the adaptive advantage oftidal rhythms in a deep water crab. Aschoff (1964) maintains that a physiological oscillatory mechanism confers an advantage in its own right. The periodic increases in amplitude allow, at certain times, higher levels of energy expenditure and hence of efficiency (alternating with low-level quiescent periods) than could be achieved by a nonoscillating system for the same overall expenditure of energy. The most obvious advantage in energy conservation would result from having this oscillation correctly synchronized with environmental changes. For the most vulnerable period of the cycle, the dormant animal, usually hidden, is not available to predators, and is active at the same time as its principal prey. This results in the conservation of energy and its concentration into a smaller time period. Activity rhythms also result in temporal partitioning of the environment, thereby increasing its usage. In Fogarty's work (using photoperiod), and in the present study (utilizing constant conditions), the level of locomotor activity was low throughout the testing period (Figs. 3 and 4). Fogarty speculated that, in his inshore study locale, the presence of low-level activity during the photophase in C. irroratus, and the total lack of daytime activity observed in C. borealis, might serve as temporal partitioning offoraging sites and permit the division offood resources. However, because of the much greater magnitude of nocturnal activity exhibited by both species, this contention is not easy to support. When the mean hourly activity (MHA) was calculated for the DD tests based on a 24-h day, it appeared to indicate a low-level, sporadic, non-rhythmic activity (Figs. 3B and 4B). When the MHA was recalculated using 25-h days, it appeared that each "tidal day" was separated by the crabs into two periods, one of high activity and one oflow activity. It is difficult to explain why the two tests appear to be mirror images of each other, though the two samples were collected and tested 6 months apart. Another possible advantage of the tidal rhythm is related to the timing of seasonal movements inshore which commence in October or November. Shotton (1973) postulates that C. irroratus may follow shifting isotherms as the inshore water cools but emphasizes that there is no direct evidence to support the suggestion. An alternative explanation is that the tidal rhythm, repeating at regular intervals, can be used as a timekeeping mechanism and that seasonal changes in intensity related to positional changes of celestial bodies provide information that triggers their inshore movements. Brittle stars (Tyler and Gage, 1979) and several benthopelagic fish (Gordon, 1979) exhibit annual reproductive cycles at depths of 2,000-3,000 m in the apparent absence of seasonal stimuli. An endogenous timer has been postulated. Timing mechanisms also allow for the utilization of time-compensated cues in migration (Rebach, 1983). An endogenous timing mechanism would enable the rock crab to anticipate fluctuations of the environment without constant monitoring. A final possibility is that this rhythmicity is an ecological or evolutionary remnant of times when the population lived in shallow water. Fogarty's work on inshore populations, in which a photoperiod was presented, found only a solar periodicity. Most work performed on shallow water crabs indicates the presence of tidal rhythmicity. In the present study, this rhythmicity was suppressed in the presence of photoperiodic stimuli. If Fogarty's presentation of photoperiodic cues to New England populations maintained in non-tidal conditions also suppressed an underlying tidal periodicity, then it is possible that the tidal rhythmicity is of no biological significance in deep water in the mid-Atlantic population. It is doubtful that the crabs move inshore/offshore on a perfectly horizontal path each season, especially since bottom currents (which may affect their movements)

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reverse seasonally. Thus, there may be interchange between populations at different locations throughout their range. This tidal rhythmicity may, therefore, be a result of previous years spent in shallow waters. Naylor (1963) found that C. maenas retained the ability to exhibit persistent tidal rhythms (which were reinitiated by periodic chilling) even when kept in non-tidal conditions. If there is little interchange between populations, the persistent tidal rhythms may also be a manifestation of their shallow water ancestry. If there is an advantage to concentrating their activity at those depths, few cues are available, and it is not unreasonable to find populations that have been entrained to tidal features which are the primary cue in the habitat of the rock crab in the mid-Atlantic region. ACKNOWLEDGMENTS I thank Dr. T. Sawyer of the NOANOxford NMFS laboratory and the VIMS Wachapreague field station for supplying many of the crabs, P. Randall for helping design the equipment, P. Feeney, F. von Staden and J. Stribling for help in reducing the activity data, D. Mignogno and J. Stribling for the preparation of the figures, the University of Maryland Computer Center for partial support of the data analysis and Drs. W. Bell and E. Bass for helpful discussions. This research was supported by USDA/CSRS grants No. 316-15-127 and 801-15-50. LITERATURE CITED Apel, J. R., H. M. Byrne, J. R. Proni and R. L. Charnell. 1975. Observations of oceanic internal and surface waves from the Earth Resources Technology Satellite. J. Geophys. Res. 80: 875-881. Aschoff, J. 1960. Exogenous and endogenous components in circadian rhythms. Cold Spring Harbor Symp. Quant. BioI. 25: 11-28. --. 1964. Survival value of diurnal rhythms. Symp. Zool. Soc. Lond. 13: 79-98. --, ed. 1981. Handbook of behavioral neurobiology, Vol. 4, Biological rhythms. Plenum Press, New York. 563 pp. Barnwell, F. H. 1966. Daily and tidal patterns of activity in individual fiddler crabs (Genus Uca) from the Woods Hole region. BioI. Bull. 130: 1-17. Battisti, D. S. and A. 1. Clarke. 1982. A simple method for estimating barotropic tidal currents on continental margins with specific application to the M2 tide off the Atlantic and Pacific coasts of the United States. J. Phys. Ocean. 12: 8-16. Bennett, M. F., J. Shriner and R. A. Brown. 1957. Persistent tidal cycles of spontaneous motor activity in the fiddler crab, Uca pugnax. BioI. Bull. 112: 267-275. Bigford, T. E. 1979. Synopsis of biological data on the rock crab, Cancer irroratus Say. NOAA Technical Report. NMFS Circular 426. U.S. Dept. Commerce, NOAA, NMFS. 26 pp. Bregazzi, P. K. and E. Naylor. 1972. The locomotor activity rhythm of Talitrus sa/tator (Montagu) (Crustacea, Amphipoda). J. Exp. BioI. 57: 375-391. Brown, F. A., Jr. 1954. Persistent activity rhythms in the oyster. Amer. J. Physiol. 178: 510-514. -and H. M. Webb. 1948. Temperature relations of an endogenous daily rhythmicity in the fiddler crab, Uca. Physiol. Zool. 21: 371-381. --, M. F. Bennett and H. M. Webb. 1954. Daily and tidal rhythms of02-consumption in fiddler crabs. J. Cell. Compo Physiol. 44: 477-506. --, M. Fingerman, M. I. Sandeen and H. M. Webb. 1953. Persistent diurnal and tidal rhythms of color change in the fiddler crab, Uca pugnax. J. Exp. Zool. 123: 29-60. --, R. A. Brown, H. M. Webb, M. Bennett and J. Shriner. 1956. A persistent tidal rhythm of locomotor activity in Uca pugnax. Anat. Rec. 125: 613-614. Clarke, G. L. 1954. Elements of ecology. Ch. 6. Light. Pp. 185-241. John Wiley & Sons, Inc., New York. 560 pp. --. 1969. The significance of spectral changes in light scattered by the sea. Pages 164-172 in P. Johnson, ed. Remote sensing in ecology. Ch. 11. Univ. of Georgia Press, Athens, GA. Creutzberg, F. 1975. Orientation in space: animals (8.1). Invertebrates. Pages 555-655 in O. Kinne, ed. Marine ecology, Vol. 2, Physiological mechanisms, pt. 2. John Wiley and Sons, New York. DeCoursey, P. J. 1983. Biological timing. Pages 107-162 in F. J. Vernberg and W. B. Vernberg, eds. The biology of Crustacea, Vol. 7, Behavior and ecology. Ch. 3. Academic Press, New York. Enright, J. T. 1965. The search for rhythmicity in biological time-series. J. Theoret. BioI. 8: 426468.

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of Natural Sciences, University Maryland

Eastern Shore, Princess Anne.