Collapse of the Diurnal Variation Pattern of Lobster Activity and Its Causes

BULLETIN OF MARINE SCIENCE, 61(1): 129–138, 1997

COLLAPSE OF THE DIURNAL VARIATION PATTERN OF LOBSTER ACTIVITY AND ITS CAUSES

Yutaka Nagata and Takashi Koike

ABSTRACT To investigate the nocturnal habits of the Japanese spiny lobster, (Panulirus japonicus), we produced diurnal brightness changes of a 12-h light period (daytime) and a 12-h dark period (nighttime) in our tanks. Under a condition with 3.3 x 102 lux daytime brightness and 0 lux nighttime brightness (the standard condition), movements of a spiny lobster exhibited a clear diurnal pattern, almost in phase with the brightness change. However, the pattern collapses under several conditions: when the nighttime brightness was higher than a threshold value of about 1.8 x 10-4 lux (the nighttime activity was considerably suppressed); when the daytime brightness was changed from the standard value to 0 lux, the diurnal pattern was skewed and its variation period shortened and became 23 h. (By using this scheme, we determined the minimum daytime brightness recognizable by spiny lobsters to be about 2.3 x 10-5 lux); when a spiny lobster was placed in new circumstances, the activity of the lobster was considerably increased for the first few days. This increase occurs in parallel both in nighttime and in daytime activities, and a collapse of the pattern occurred not only due to external conditions but also due to internal conditions.

The Japanese spiny lobster, Panulirus japonicus, is nocturnal, and its activities are strongly controlled by underwater light levels. To investigate the diurnal patterns of lobster movement, we produced a diurnal brightness change of a 12-h bright period (daytime) and a 12- h dark period (nighttime) in our experimental tank, and observed how the diurnal pattern was affected by these conditions (Koike et al., 1995, 1996a, 1996b). The apparatus used was a simple device (Koike et al., 1997). If the daytime brightness was higher than 2.3 x 10-5 lux and the nighttime brightness was lower than 1.8 x 10-4 lux, movements of spiny lobsters exhibited clear diurnal patterns almost in phase with the brightness variation. However, the pattern was disturbed or collapsed under various conditions. Several of these conditions will be discussed. SPINY LOBSTER ACTIVITY. —Japanese spiny lobsters used in our experiments had been caught near the Shima Peninsula, Mie Prefecture. We used male lobsters of medium size, the weights of which ranged between 250 and 350 g, and carapace lengths from 7.0 to 8.5 cm. Though more than 20 spiny lobsters were used in our experiments, the magnitude of their frequency of activity (definition in Koike et al., 1997) is mainly determined by water temperature as shown in Figure 1. The activity was highest near 20° C, and tended to decrease linearly with temperature increase or decrease from this temperature. Activity frequencies of two specific lobsters are plotted against water temperature in Figure 2. One lobster (Fig. 2a) was not as active in comparison with the other (Fig. 2b), if the standard value of the threshold strain, 2 g, was selected. (We assumed that the lobster moved if the strain changed over a prescribed threshold value between successive data recordings.) We counted the frequency of activity (Koike et al., 1997). The frequency of activity of the relatively inactive lobster (Fig. 2) increased when we selected a smaller threshold value (1 g: Fig. 2, the left middle figure, and 0.5 g: Fig. 2, the lower left figure). While, the frequency of activity of the relatively active lobster (Fig. 2b) was not influenced by the threshold strain value

129 130 BULLETIN OF MARINE SCIENCE, 61(1): 129–138, 1997

Figure 1. Relation between the water temperature (°C) and the frequency of activity of the lobster Panulirus japonicus accumulated over the day when the temperature measurement was made. The data were removed when the daytime frequency of activity was higher than 400 (see the discussion).

(Fig. 2, right). Thus, the frequencies of activity of the two lobsters were almost identical when the threshold strain was selected to be 0.5 g. This suggests that the individuality of the lobsters appears in magnitude of each move, but not in frequency of activity. So, if the threshold strain value is selected to be small enough, or if only active lobsters are used, the variability of the experimental results due to lobster individuality would be minimized. However, it should be noted that we did not measure other important parameters, such as dissolved oxygen. Experimental lobsters were fed a whole mussel (Mytilus edulis) weighing about 5 g once a day. SUPPRESSION OF NIGHTTIME A CTIVITY. —Diurnal variations of the frequency of activity were examined for several levels of nighttime brightness, and are shown in Figure 3. The daytime brightness was 3.3 x 102 lux, always identical for these experiments. It is clear that the nighttime activity was considerably suppressed when the nighttime brightness was higher than 5.2 x 10-3 lux. The relationship between the frequency of activity and the nighttime brightness is shown in Figure 4. We found that the frequency of activity value for 1.8 x 10-4 lux was at the mean value between the levels in the highest activity and lowest activity regimes. An example of the temporal variations of the nighttime and daytime activities is shown in Figure 5 developed from the experiment conducted from 14 October to 8 December 1994. The daytime brightness was kept at 3.3 x 102 lux throughout the experiment. Figure 5 shows two experimental “runs” conducted successively: (1) The nighttime brightness was 0 lux for the period from day 1 to day 6 (the “standard condition”), and was lowered to 1.8 x 10-4 lux at day 7, and (2) the nighttime brightness was again set at 0 lux for the period from day 28 to day 31, and was lowered to 8.8 x 10-4 lux at day 32. The variation in the pattern in the second run was a typical for the experiments of this kind, though the nighttime activity was extremely high in the standard condition (day 28 - 32). This may suggest that the “conditioning”-period under the “standard conditions” was not long enough for this run. The lobster maintained a relatively high activity level for several days after the light condi- NAGATA AND KOIKE: DIURNAL LOBSTER ACTIVITY 131

Figure 2. Relation between the water temperature (°C) and the frequency of activity of the lobster Panulirus japonicus accumulated over each night for two specific lobsters (a: left) and (b: right). The measured temperature range was from about 7 to about 16° C. We assumed that the lobster moved if the strain change of one of the supporting wires exceeded a prescribed threshold value, and counted the frequency of the lobster movements. Three threshold strain values, 2 g (the standard value: upper figures), 1 g (middle figures) and 0.5 g (lower figures) were applied.

tion was changed (this behavior discussed later), but its activity gradually decreased to- ward a constant value. However, the behavior of the lobster in the first run was rather strange. The lobster activity in the last few days of the conditioning period (day 7 - 9) was normal, and showed a typical value usually seen in the standard condition (Fig. 4). After the light level was changed, the lobster maintained its activity at the same level as in the standard condition (day 8 - 15). Then, the activity level became lower, and during day 18 - 21 corresponded to that in the inactive regime (Fig. 4). However, the level increased again to that in the active regime at the end of this run (day 26 - 28). The averaged activity in this case at a light level of 1.8 x 10-4 lux was located at just the middle between the active and inactive regimes as seen in Figure 4. It would be reasonable to think that the activity level was occasionally shifted between the active and inactive levels in this case, and this nighttime brightness was near a threshold value separating the active and inactive regimes. Namely, the lobster appeared to be con- fused by this light level at night: it judged sometimes that this brightness was too high to move, but at other times that it was low enough to move around. It is reported that Japanese spiny lobsters cannot be caught on nights of the full moon (Kubo and Ishiwata, 1964 and Yoza et al., 1977). The underwater brightness at the depth of about 15 m off the Shima Peninsula on the full-moon night (Maegawa, pers. comm.) is 132 BULLETIN OF MARINE SCIENCE, 61(1): 129–138, 1997

Figure 3. Typical diurnal behavior patterns of the lobster, Panulirus japonicus, obtained for the various nighttime brightness-levels: a) 0 lux (25 November 1992), b) 2.3 x 10-5 lux (17 April 1992), c) 5.2 x 10-3 lux (5 May 1992), d) 3.5 x 10-2 lux (16 May 1992), and e) 2.0 lux (6 July 1992). The daytime brightness-level was kept at 3.3 x 102 lux in these experiments. NAGATA AND KOIKE: DIURNAL LOBSTER ACTIVITY 133

Figure 4. Dependence of the lobster, Panulirus japonicus, activities (frequency per hour) in daytime (white circles) and in nighttime (black circles) on the nighttime brightness-level (lux). The daytime level was kept at 3.3 x 102 lux in these experiments.

Figure 5. Temporal variations of the daytime activity (white circles) and nighttime activity (black circles). The frequency of activity per hour averaged over each daytime or each nighttime is taken in the ordinate. The daytime brightness-level was kept to be 3.3 x 102 lux throughout the experiment. The figure shows two experimental runs conducted successively: (1) The nighttime brightness-level was 0 lux from day 1 to day 6, and was lowered to 1.8 x 10-4 lux on day 7, and (2) the nighttime brightness-level was again set at 3.3 x 102 lux from day 28 to day 31, and was lowered to 8.8 x 10-4 lux on day 32. 134 BULLETIN OF MARINE SCIENCE, 61(1): 129–138, 1997

Figure 6 (left). Temporal variations of the diurnal pattern in an experimental run conducted from 28 May to 2 July 1993: the lobster was kept in the standard condition for the first 7 d (indicated with circled day numbers in on the left side of each figure). From day 8, the daytime brightness-level was set at 0 lux, and the lobster was kept in pitch dark thereafter (Koike et al., 1996b). Figure 7 (right). Same as in Figure 6 except in an experimental run conducted from 21 September to 31 October 1993, and except that the daytime brightness-level was set at 2.3 x 10-5 lux from day 8. NAGATA AND KOIKE: DIURNAL LOBSTER ACTIVITY 135

Figure 8. Diurnal patterns observed from 26 June through 31 July 1995. The lobster molted in the period between 23 July and 25 July, but its exact time was not recorded.

estimated to exceed the threshold value (1.8 x 10-4 lux) obtained in our experiments. Arechiga and Atkinson (1975) reported that the burrowing Norway lobster, Nepherops norvegicus, come out from their caves when the underwater light level is lower than 10-5 lux. The value roughly corresponds to our result. DECREASE OF THE VARIATION PERIOD FOR THE LOW DAYTIME BRIGHTNESSES. —After keeping the lobster in the “standard condition” for several days, the daytime brightness-levels were changed to several prescribed levels in a series of our experiments, and the change in the 136 BULLETIN OF MARINE SCIENCE, 61(1): 129–138, 1997

diurnal pattern of the lobster movement was investigated. An example of the temporal change in the pattern is shown in Figure 6 for the case in which the daytime brightness-level was lowered to 0 lux. The first 7 d was the conditioning period in the standard condition, and the daytime brightness-level was 0 lux after day 8. The variation pattern remained unchanged from day 8 to day 11. However, from day 12 the transition time from the inactive period (originally corresponding to daytime) to the active period (originally corresponding to nighttime) began to shift forwards day by day. This phase shift continued until day 23, and the diurnal variation period for these days was 23 h (Koike et al., 1996b). Such a shift in phase was not recognized after day 24, and the variation period appeared to return again to 24 h. However, the diurnal pattern itself became somewhat ambiguous for these later periods. The clear phase shift occurred when the daytime brightness level was lowered to the levels lower than 6.8 x 10-8 lux, but never occurred when lowered to the levels higher than 5.2 x 10-3 lux. Another example of the temporal change of the pattern is shown in Figure 7 for the case in which the daytime brightness-level was lowered to 2.3 x 10-5 lux. The lobster was also kept in the standard condition from day 1 to day 7 in this case. From day 8 to day 11, the diurnal pattern was disturbed, and relatively high activity was observed even in daytime (especially for day 8 and day 9; this disturbance will be discussed later). The forward shift of the transition time from active to inactive periods appeared to occur during the period from day 12 to day 14. But, the transition time returned to 17:00 (in phase with the brightness change) on day 15. The forward shift was observed also in the period from day 15 to day 18, but the transition time came in phase again on day 19. This result suggests that the lobster identifies the 2.3 x 10-5 lux more or less as daytime. Thus, we may conclude that the minimum daylight brightness recognizable by spiny lobsters is about 2.3 x 10-5 lux. Similar phase shifts of the diurnal variation pattern after the daytime brightness-levels were lowered were reported for cat fishes, Silurus asotus by Tabata (1992) and for hagfishes, P. atami and E. burgeri by Kabasawa and Ooka-Souda (1991). The threshold brightness value obtained here is about 12.5% of the threshold value, above which the nighttime lobster activity is suppressed. Powers and Barlow (1985) reported that the eye sensibility of the horseshoe crab Limulus was 10 times greater in nighttime than in daytime. Further investigations would be needed to understand the discrepancy between two threshold brightness values. DISTURBANCES IN THE DIURNAL PATTERN WHEN THE LOBSTERS WERE PUT INTO A NEW ENVI- RONMENT. —When Japanese spiny lobsters were first put into the experimental tank, they were usually disturbed and moved around actively for several days. Examples of such acti- vation can be seen on day 2 and day 3 in Figure 6. Similar anomalous lobster activity happens when the lighting conditions are changed. Typical examples are seen on day 33 through day 37 in Figure 5, and on day 8 and day 9 in Figure 7. (The enhancement on day 33 - 37 in Figure 5 would be partly influenced by the extremely high activity on day 29 - 32 which resulted from the shortness of the conditioning period.) As seen in these examples, one of the characteristics of this kind of disturbance is that the enhancement occurs not only in the nighttime activity but also in the daytime activity. The effects of such anomalous enhancement on the experimental results may be removed by invoking the idea that the daytime activity increases in parallel to the nighttime activity. We omitted such anomalous data when we analyzed the correlation between the frequency of activity and the water temperature shown in Figure 1. NAGATA AND KOIKE: DIURNAL LOBSTER ACTIVITY 137

COLLAPSE OF THE DIURNAL PATTERN AT THE TIME OF MOLTING. —A collapse of the diurnal pattern of lobster movement would occur not only due to external light conditions men- tioned above but also due to the “internal” conditions of spiny lobsters. We have not inten- tionally investigated such disturbance or collapse of the diurnal pattern due to internal conditions, but we observed an unusual diurnal pattern at the time of molting. An example is shown in Figure 8 from the experiment conducted from 26 June through 25 July 1995. The lobster molted during the period 23 and 25 July. The frequency of activity dropped considerably more than 20 d before the molting. The activity was especially small from 23 June through 25 July. One of the characteristic features is the increase of daytime activity rela- tive to nighttime activity. For about 1 wk before the molting (on 17 through 23 July), the daytime activity had almost the same magnitude as the nighttime activity, and the diurnal pattern collapsed almost completely. Nighttime activity recovered a few days after the molting (from the night of 26 July). However, the daytime activity was high for several days (say, from 26 through 30 July). It appears that the lobster was in a state of excitement after molting, and that it behaves as just as in the case of the circumstance change discussed in the previous sub-section. This indicates that a collapse of the pattern occurs not only due to external conditions but also due to internal conditions. We believe that investigations into the diurnal variation pattern and the phenomenon of its collapse are necessary to understand the behavior of a spiny lobster.

ACKNOWLEDGMENTS

The authors wish to express their thanks for the staffs of the Fisheries Research Laboratory of the Mie University for their valuable assistance. The research was supported partly by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science and Culture of Japan, and by a research grant from the Kakushin Foundation of Research and Education.

LITERATURE CITED

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Yoza, K., K. Nomura and H. Miyamoto. 1977. Observations upon the behavior of the lobster and the top-shell caught by bottom-set gillnet. Bull. Japan. Soc. Sci. Fish. 43: 1269-1272 (in Japanese).

DATE ACCEPTED: October 15, 1996.

ADDRESS: Faculty of Bioresources, Mie University, 1515 Kamihama, Tsu, Mie 514, Japan.