Sesarma Erythrodactylum Masayuki Saigusa Department of Biology

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Sesarma Erythrodactylum Masayuki Saigusa Department of Biology Benthos Research Vol.52, No.1: 21-33 (1997) BENTHOS RESEARCH The Japanese Association of Benthology The circatidal clock of an estuarine semi-terrestrial crab, Sesarma erythrodactylum Masayuki Saigusa Department of Biology, Faculty of Science, Okayama University ABSTRACT The influence of the tidal cycle decreases with the distance from the sea, and this may af- fect the behavioral timing systems in estuarine animals. In addition, the circatidal rhythm of these animals may be controlled by light-sensitive systems. To investigate the timing systems in estuarine animals, the larval release activity of a semi-terrestrial crab, Sesarma erythrodactylum, was monitored in the laboratory without any tidal influence. The larval release rhythm free-ran under constant dim light conditions, which suggests that the tim- ing of release is under the control of an endogenous clock. The free-running period was somewhat different for each individual. Under an artificial 24-h light-dark (LD) cycle in phase with that in the field, the timing of release coincided with high tides at night. In con- trast, the rhythm changed to match a phase-shifted 24-h cyclic light regimen. These results demonstrate that a light-sensitive mechanism is certainly involved in the circatidal timing systems of S. erythrodactylum. The role of the 24-h LD cycle is not only to shift the syn- chrony of the timing of release onto the other high tide when necessary for maintaining a nocturnal schedule, but also to drive the phase of the circatidal rhythm. While the tidal be- havioral rhythms of intertidal animals reflect two parameters of the tidal cycle, i, e., the 12.4-h period and the tidal amplitude, those of estuarine crabs lose synchrony with the tidal amplitude and show a nocturnal pattern instead. These properties of the circatidal rhythm of larval release in S. erythrodactylum and other intertidal and estuarine crabs can be ex- plained by a coupled oscillator hypothesis. Key words: larval release, estuary, crab, Sesarma erythrodactylum, nocturnal, circatidal rhythm, zeitgeber, coupled oscillator INTRODUCTION Barlow et al. 1986; Saigusa & Akiyama 1995). Some of these patterns are clearly under the In the intertidal and estuarine environments, control of endogenous clocks (Klapow 1972; the lives of organisms are strongly restricted Enright 1976; Hastings 1981), but other pat- spacially and temporally by the tidal cycle. A terns are caused by the direct response of the number of organisms synchronize their activi- animals to cyclical fluctuations of physical fac- ties with this predictable cycle in the environ- tors correlated with tides (e.g., Honegger 1973; ment and show complex activity patterns syn- Lehmann 1976; Reid & Naylor 1990; Northcott chronized with not only the day-night cyle but et al. 1991). also the tidal cycle (Saigusa 1981, 1982, 1985; One of the main problems in tidal rhythm re- search is the relationship between the rhythmic Received September 13 , 1996 : Accepted January 27, 1997 pattern and the tidal influence. The tidal cycle 21 Vol.52,No.1 Benthos Research June,1997 is characterized by two kinds of physical pa- rhythm in each female. The 12.4-h tidal rhythm rameter; i.e., the mean period length of 12.4-h, for larval release in the coastal terrestrial crab and the semidiurnal inequality of the tidal Sesarma pictum also exhibits the properties height. Intertidal animals may possess timing very similar to those of S. haematochier systems that can respond to both parameters, (Saigusa 1992) . Even in the intertidal crab as exemplified by the swimming activity of Hemigrapsus sanguineus, the circatidal rhythm some amphipods and isopods (Enright 1963; responds to 24-h light cycles with phase shifts Klapow 1972), the mating behavior of a horse- (Saigusa & Kawagoye 1997). shoe crab (Barlow et al. 1986), emergence in a Thus, the circatidal timing systems clearly midge (Saigusa & Akiyama 1995), and larval contain a light-sensitive mechanism. Further release of a grapsid crab (Saigusa & Kawagoye evidence for this would be useful for under- 1997). In contrast, synchrony with the inequal- standing circatidal timing systems. This study ity of the tidal amplitude may not be of great reports the larval release activity of an advantage to the estuarine animals, including estuarine semi-terrestrial crab, Sesarma those living in the terrestrial habitat. Accord- erythrodactylum, monitored in the laboratory, ingly, the animal's tidal rhythm of behavior and discusses the tidal timing systems in may reflect only the 12.4-h (or 24.8-h) interval estuarine crabs. of the tides. Another problem is the light-sensitive sys- MATERIALS AND METHODS tems that are involved in the circatidal rhythms. Palmer (1995) supposed that day- Distribution of estuarine crabs in relation to night cycles can entrain only the circadian salinity fluctuations and tidal amplitude rhythms, and that they cannot be the entrain- The distribution of estuarine crabs is closely ing agent for circatidal rhythms. Most tidal related to salinity, substrate, and fluctuations rhythms reviewed by Palmer (1995) are related in water level (e.g., Ono 1965) . The habitats of to activities in which internal timing systems Sesarma erythrodactylum and other species of are not clearly participating, e.g., locomotor crabs were surveyed along a small river at activity patterns of fiddler crabs (Honegger Kasaoka, Okayama Prefecture, Japan (see 1973; Lehmann 1976), those of a shore crab also Saigusa 1982) . This investigation was made (Bolt et al. 1989; Reid & Naylor 1990), and the by visual inspections many times over the last swimming activity patterns of a fish (Northcott 15 years. et al. 1991) . Such activity patterns make it diffi- cult to evaluate how an environmental cycle en- Collection of ovigerous females and mainte- trains the internal timing systems. nance in the laboratory In contrast, the larval release activity pat- Ovigerous females were collected from the field terns of many estuarine and intertidal crabs (Fig. 2) in June and July in 1991-1996. They are controlled endogenously, and for some were brought into the laboratory and placed in crabs there are unequivocal evidence that the aquaria (70 cm long, 40 cm wide, and 25 cm circatidal rhythms respond to 24-h light-dark high). Each aquarium held a shallow pool of di- (LD) cycles. For example, an estuarine terres- luted seawater (salinity about 2O%), and hiding trial crab, Sesarma haematocheir, exhibits a places made of boards were set above the sur- nocturnal tidal rhythm (Saigusa 1981, 1982). face of the water. The crabs were fed every few This rhythm becomes desynchronized among days. The experimental rooms in the labora- individuals in constant darkness, but is main- tory were equipped with controlled light and tained for at least 3 weeks under a 24-h LD temperature. Temperature was 24•}1•Ž . Light cycle. In addition, this rhythm is easily phase- intensity was about 700-1200 lux at the floor shifted under a 24-h LD cycle changed in phase with the lights-on, and less than 0.01 lux with from that in nature (Saigusa 1986). The close the lights-off. Three experiments were carried correlation between the phase shift in the be- out under continuous light at 0.5-1.0 lux. havioral rhythm and this light cycle suggests The day of hatching is difficult to predict; the that the 24-h LD cycle sets the phase of the tidal only indication that hatching is imminent is the 22 Larval release of an estuarine crab brownish green color of the embryos (mainly after being confined in the recording appara- caused by yolk consumption). The embryos of tus. each female were checked by eye every day, and The experimental procedures for S. those crabs carrying embryos that seemed erythrodactylum were basically the same as likely to hatch within a few days were each set those for S. haematocheir and S. pictum, and individually in a recording apparatus placed in they have already been described elsewhere the same room (Fig.1A). With this apparatus, (Saigusa 1986, 1992). A 500ml glass beaker (8.5 the time of larval release could be monitored cm in diameter, 12cm high) was used to hold without any change in the ambient lighting con- the crab's plastic cage (Fig.1A). Because the ditions (e.g., without switching on a red light to ovigerous females of S. erythrodactylum have a monitor the release) (Fig.1B). much smaller carapace (0.8-1.5cm) than that of S. pictum, the amount of seawater was re- Monitoring of larval release activity duced to 160-170ml. The number of ovigerous The larval release recording system consisted females used in each experiment is described in of a sensor unit (infrared source and receiver: the text. Some females were released into the E3S-2E4, Omron Co. Ltd., Japan) placed inside aquaria before being confined in cages. Fur- the experimental room and a control unit (S3S- thermore, sometimes the photoelectric switch A10, Omron) and event recorder (R17-H12T, did not operate because the number of hatched Fuji Electric Co. Ltd., Japan) placed outside. zoeas was very few. Because the time of the re- Each ovigerous female was confined in a small lease in such cases was not recorded, they were plastic cage (6.5cm in diameter and 6.5cm excluded from the analyses. high) with many holes drilled in the sides and bottom. As shown in Figure 1A, this cage was RESULTS suspended by fine wires from the rim of a glass beaker containing diluted, clean seawater (sa- Habitat of crabs in the estuary linity about 20•ñ). The animals were not fed Sesarma erythrodactylum exclusively inhabits Fig.1 . System for recording the larval release activity of Sesarma erythrodactylum females. A. The apparatus used to detect the time of day of larval release . w: fine wire.
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