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Diurnal migrations of the echinoid Diadema setosum (Leske)
DIURNAL MIGRATIONS OF THE ECHINOiD Diadema setosum (Leske) BY I. W. B. T H O R N T O N *
University College of Khartoum, Sudan The island of Suakin stands in a lagoon connected to the open sea by a narrow channel atmost a mile long. The natural harbour thus formed is no longer used except by a few small native craft during the pilgrim season. The low-lying island is bounded by a cliff which drops half a metre to the water surface and a further one to three metres to the bottom. A search of the sea bed near the island during the day reveals only very occasional specimens, but the tips of the spines of many individuals can be seen in the crevices of the cliff face. At night, the urchins emerge on t o the adjacent sea bed, and their dark shapes can be spotrighted with a powerful lamp, when they move out of the beam immediately.
Introduction
Millot (1954) has performed a series of experiments on the responses of Diadema antillarum Philippi to directional light and to changes in light intensity, concerning movements both of the whole animal and of isolated organs. In a study of the effect of change in right intensity on the movement of the whole animal, he has demonstrated that the response depends on the light intensity to which the urchin has been subjected for the period immediately preceding the change. Thus a dark-adapted animal avoids light of increased intensity, and a light-adapted one moves away from shade when the intensity of light is reduced. The response is most marked in dark-adapted urchins. Millot suggests that the nervous system, which he has shown to be directly excited by light, is shielded during the day by pigment in superficial melanophores and relatively exposed at night, the animal then responding to very small changes in light intensity Observations and experiments of the related Table I. Numbers of D .
setosum
Observations and Experiments
For two twenty-four hour periods during 15th18th December, 1955, a section of the cliff face, 30 metres long, and its adjacent sea bed to a distance of 3 metres from the shore were kept under observation, and counts were made every two hours of all visible urchins. The tabulated
Observed in Various Situations at Intervals ThroughoutTwo Periods of Twenty-four Hours
17/18.xii.55
15/16.xii.55 Tip.s of sprees visible
LocalTime Noon 14.00hrs. 16.00 17.15 17.20 17.30 18.00 18.30 20.00 22.00 24.00 02.00 O4.00 05.00 05.30 06.00 08.00 I0.00 Noon
Test fully exposed
In On cliff On sea crevices face bed 37 0 0 32 0 0 35 0 0 5 38 1 DUSK 17 44 25 2 41 67 3 39 71 4 41 83 0 41 81 0 42 82 0 43 83 0 42 78 0 40 75 DAWN 41 0 0 34 0 0 38 0 0 36 0 0
Tips of sprees
Test fully exposed
visible In On cliff On sea crevices face bed 36 0 0 Gusty, no cloud 35 0 0 39 0 0 10 27 0 DUSK 6 42 21 Wind dropped. Moon 1 40 70 4 45 68 0 43 82 Moon gone 0 41 86 0 42 84 0 42 78 0 44 82 0 41 76 DAWN 38 0 0 No sun 36 0 0 Sun 37 0 0 37 0 0
Weather
Weather
Calm, no cloud
No moou, calm
Sun
figures (Table I) show that a definite nocturnal migration takes place, the urchins moving out on to the sea bed at dusk, and back into the crevices of the cliff at dawn.
species Diadema setosum (Leske) are described below. This echinoid occurs in numbers at Suakin on the Red Sea coast of the Sudan. *Now at Biology Department, Itong Kong University. 143
i44
THE
BRITISH
JOURNAL
OF
Another colony of 27 urchins in the middle o f the southern arm of the lagoon was :found at night scattered over the sea bed, but retired by day under some submerged metal plates, not a single individual being found on the exposed sea bed. This activity was observed on both dark and moonlight nights. Fox (1924) showed that the breeding rhythms of D . s e t o s u m are correlated with the lunar cycle, the gonads maturing between the first quarter and the full moon, when spawning takes place. He gives the breeding season of this species at Suez as ending in September independently of temperature. Since m y observations were made 1-4 days after the December new moon, it seems most unlikely that this activity is due to spawning rhythms. To find to what extent change in light intensity is responsible for this activity, a series of simple experiments was performed on the sea bed. Six openwork baskets made of palm branches, each containing six urchins, were suitably weighted and sunk to a depth of one metre. The mesh of the baskets was approximately four square inches, so that sea water circulated freely through them. One half of each basket was shaded and the position of the shaded half alternated in the six baskets. Records of the positions of the urchins at two-hour intervals were made over two periods of twenty-four hours. The results (Table II) show that the urchins, which were collected from crevices at 11.30 hours, quickly moved into the shade, Table H.Number of D . s e t o s u r a in
ANIMAL
BEHAVIOUR,
iV,
4
remained there until dusk, and then emerged into the exposed half. After 20.00 hours, some of them moved back into the shaded half, the distribution of urchins in the two halves after that time being evidently random until dawn when all moved into the shaded half. Unequal distribution of food organisms or dissolved oxygen may thus be discounted as causative factors of the nocturnal migrations. The activity of the captive urchins differs from that of the natural population only in the return of some of the animals to the shade after 20.00 hours. This may be the result of random movement in a confined space, which would not occur in the natural population. Diurnal changes in food distribution, dissolved oxygen, current speed and temperature, as well as some inherent rhythm, may equally well account for the results shown in Tables I and II. Further experiments were thus designed to establish the relative importance of change in light intensity and any of these, as causative factors. Six urchins were kept in each of four fully exposed baskets until midnight when one half of each basket was shaded, the urchins being in the exposed halves. In two baskets the exposed half was illuminated, the intensity of illumination being 40 foot-candles. The urchins in these baskets quickly moved out of the increased illumination into the shaded half (Table III), whereas in the controls only very few did so, and more slowly. In a similar experiment, in which six urchins were kept in each of six completely shaded baskets during
the Exposed Half of Each of Six Haft-shaded Baskets, at Intervals Throughout Two Periods of Twenty-four Hours
Local Time Noon 12.15 hrs. 14.00 16.00 17.15 17.20 17.30 18.00 20.00 22.00 24.00 02.00 04.00 05.00 05.30 06.00
08.00 10.00 Noon
17/18.xii.55 6 6 6 1 0 0
6 0
6 0
0 0 0
0 0 0
5 6 6 5 4
3 5 6 6 5
DUSK 3 2 4 6 6 6 4 6 2 3
4 0
3
1 3
2
0 4
1 0 0 0
0 0 0 0
0 0 0 0
0 0 0
0 0 0
6 0
0 0 0
0 0 0
1 4 4 5 4
2 5 6 5 0
5 2
2 3
1 0 0 0
3 4 DAWN
6 0 0 0 0
6 0 0 0 0
4 6 6
4 5 6
18/19.xii.55. 6 6 6 0 0 0 0 0 0 0 0 0 0 0 0 DUSK 3 2 4 4 5 6 6 6 6
6 0 0 0 0 1 6 6
5
4
4
2
3
4
2
3 5
4
2 1 3 4
4 2 0 2
1 3 3 1
3 2 6 5
2 5 4 3
2 4 4 2
0 0 0 0
0 0 0 0
0 0 0 0
0 0 0 0
0 0 0 0
1 0 0 0
0 0 0 0
0 0 0 0
DAWN
THORNTON: DIURNAL MIGRATIONS OF THE ECHINOID DIADEMA SETOSUM (LESKE) Table IlL Number of Dark-adapted Urchins in the Exposed Half of each of Four Half-shaded Baskets, two of which were Illuminated in the Exposed Half after Midnight
6 0 0
24.00 hrs. 00.30 ,, 01.00 ,,
Light
No Light 6 6 5 4 3 4
6 0 0
the morning, and then three baskets halfshaded and three fully exposed at midday, the urchins in the half-shaded baskets quickly moved into the shade (Table IV). Table IV. Numbers of dark-adapted Urchins in the Exposed Halves of Three Half-shaded Baskets, and in the Original Halves of Three Fully Exposed Baskets
Halfshaded 6 6 6 0 0 0
12.00 hrs. 12.30 ,, 13.00 ,,
0
0
0
Fully
exposed 6 6 6 5 3 6 3 4 3
The complementary experiment was made in which urchins were kept in direct sunlight for two hours and then six of the nine containers half-shaded. The urchins in three of the halfshaded baskets were originally in the exposed half, those in the other three were originally in the shaded half. Those animals originally in the exposed half tended to stay there, while of those originally shaded, some moved into the exposed half (Table V). D i s c u s s i o n and C o n c l u s i o n
The movement away from increased light intensity by dark-adapted animals can be induced experimentally at times other than dawn, and it is probable that in the natural conditions of Suakin lagoon change in light intensity is responsible for the movement of urchins at dawn. There is some experimental evidence of the avoidance of shade by lightadapted individuals, but the response does not
145
seem to be sufficiently well marked wholly to account for the observed nocturnal redistribution of the natural populations. However, this factormay act in combination with others, resulting in the nightly migrations. It is possible that when the light intensity is reduced the effect of other stimuli, notably hunger, is added, causing the urchins to move out into the open. In the natural population the presence of food on the sea bed would tend to keep the animals there until the light factor was reintroduced at dawn. The more marked sensitivity of dark-adapted animals has been noted by Millot in his studies on the responses of D. antillarum to changes in light intensity, both concerning the spine reflex (Millot, 1953, 1954), and movements of the whole animal (Millot, 1954). It is possible that the diurnal screening effect of superficial pigment which he postulates for this species (Millot, 1950, 1952, 1953, 1954), also occurs in D. setosum. In the West Indies, D. antillarum, while commonly found in shady situations during the day, may nevertheless occur in appreciable numbers fully exposed to tropical sunlight in a few inches of water. The behaviour of D. setosum at Suakin differs from that of D. antillarum in showing a more marked avoidance of light during the day. Professor Millot has suggested to me that D. setosum may have a more developed photosensory system or be less welt protected. It is also possible that the Suakin lagoon, where the calm shallow water covers a relatively smooth sea bed on which no shadows are cast during the day, approaches experimental conditions more closely than the West Indian habitat. The relative lack of temporarily shaded sites on the sea bed at Suakin would make gradual hght-adaptation less likely, with the result that fewer urchins would be found in exposed situations during the day. Observations on both species f r o m other areas would be of great interest.
Table V. Numbers of Light-adapted Urchins in the Exposed Halves of Six Half-shaded Baskets, and in the Original Halves of Three Fully Exposed Baskets
Half-shaded
Urchins originally 12.00 hrs. 12.30 ,, 13.00 ,,
6 5 4
exposed
6 6 5
6 6 3
Urchins originally shaded 6 6 6 3 1 2 2 2 1
Fully exposed 6 6 6
6 5 5
6 6 6
i46
THE
BRITISH
JOURNAL
OF
REFERENCES
Fox, H. M. (1924). Lunar periodicity in reproduction. Proc. roy. Soe. B., 95, 523-50. Millot, N. (1950). The sensitivity to light, reactions to shading, pigmentation, and colour change of the sea urchin, Diadema antillarum Philippi. BioL Bull., Woods Hole, 99, 329-30. Millot, N. (1952). Colour change in the echinoid, Diadema antillarum Philippi. Nature, Lond., 170, 325-6.
ANIMAL
BEHAVIOUR,
iV,
4
Millot, N. (1953). Light emission and light perception in species of Diadema. Nature, Lond., 171, 973. Millot, N. (1954). Sensitivity to light and the reactions to changes in light intensity of the echinoid Diadema antillarum Philippi. Phil. Trans. roy. Soc., B., 238, 187-220. Accepted for publication 14th February, 1956.
University College of Khartoum, Sudan The island of Suakin stands in a lagoon connected to the open sea by a narrow channel atmost a mile long. The natural harbour thus formed is no longer used except by a few small native craft during the pilgrim season. The low-lying island is bounded by a cliff which drops half a metre to the water surface and a further one to three metres to the bottom. A search of the sea bed near the island during the day reveals only very occasional specimens, but the tips of the spines of many individuals can be seen in the crevices of the cliff face. At night, the urchins emerge on t o the adjacent sea bed, and their dark shapes can be spotrighted with a powerful lamp, when they move out of the beam immediately.
Introduction
Millot (1954) has performed a series of experiments on the responses of Diadema antillarum Philippi to directional light and to changes in light intensity, concerning movements both of the whole animal and of isolated organs. In a study of the effect of change in right intensity on the movement of the whole animal, he has demonstrated that the response depends on the light intensity to which the urchin has been subjected for the period immediately preceding the change. Thus a dark-adapted animal avoids light of increased intensity, and a light-adapted one moves away from shade when the intensity of light is reduced. The response is most marked in dark-adapted urchins. Millot suggests that the nervous system, which he has shown to be directly excited by light, is shielded during the day by pigment in superficial melanophores and relatively exposed at night, the animal then responding to very small changes in light intensity Observations and experiments of the related Table I. Numbers of D .
setosum
Observations and Experiments
For two twenty-four hour periods during 15th18th December, 1955, a section of the cliff face, 30 metres long, and its adjacent sea bed to a distance of 3 metres from the shore were kept under observation, and counts were made every two hours of all visible urchins. The tabulated
Observed in Various Situations at Intervals ThroughoutTwo Periods of Twenty-four Hours
17/18.xii.55
15/16.xii.55 Tip.s of sprees visible
LocalTime Noon 14.00hrs. 16.00 17.15 17.20 17.30 18.00 18.30 20.00 22.00 24.00 02.00 O4.00 05.00 05.30 06.00 08.00 I0.00 Noon
Test fully exposed
In On cliff On sea crevices face bed 37 0 0 32 0 0 35 0 0 5 38 1 DUSK 17 44 25 2 41 67 3 39 71 4 41 83 0 41 81 0 42 82 0 43 83 0 42 78 0 40 75 DAWN 41 0 0 34 0 0 38 0 0 36 0 0
Tips of sprees
Test fully exposed
visible In On cliff On sea crevices face bed 36 0 0 Gusty, no cloud 35 0 0 39 0 0 10 27 0 DUSK 6 42 21 Wind dropped. Moon 1 40 70 4 45 68 0 43 82 Moon gone 0 41 86 0 42 84 0 42 78 0 44 82 0 41 76 DAWN 38 0 0 No sun 36 0 0 Sun 37 0 0 37 0 0
Weather
Weather
Calm, no cloud
No moou, calm
Sun
figures (Table I) show that a definite nocturnal migration takes place, the urchins moving out on to the sea bed at dusk, and back into the crevices of the cliff at dawn.
species Diadema setosum (Leske) are described below. This echinoid occurs in numbers at Suakin on the Red Sea coast of the Sudan. *Now at Biology Department, Itong Kong University. 143
i44
THE
BRITISH
JOURNAL
OF
Another colony of 27 urchins in the middle o f the southern arm of the lagoon was :found at night scattered over the sea bed, but retired by day under some submerged metal plates, not a single individual being found on the exposed sea bed. This activity was observed on both dark and moonlight nights. Fox (1924) showed that the breeding rhythms of D . s e t o s u m are correlated with the lunar cycle, the gonads maturing between the first quarter and the full moon, when spawning takes place. He gives the breeding season of this species at Suez as ending in September independently of temperature. Since m y observations were made 1-4 days after the December new moon, it seems most unlikely that this activity is due to spawning rhythms. To find to what extent change in light intensity is responsible for this activity, a series of simple experiments was performed on the sea bed. Six openwork baskets made of palm branches, each containing six urchins, were suitably weighted and sunk to a depth of one metre. The mesh of the baskets was approximately four square inches, so that sea water circulated freely through them. One half of each basket was shaded and the position of the shaded half alternated in the six baskets. Records of the positions of the urchins at two-hour intervals were made over two periods of twenty-four hours. The results (Table II) show that the urchins, which were collected from crevices at 11.30 hours, quickly moved into the shade, Table H.Number of D . s e t o s u r a in
ANIMAL
BEHAVIOUR,
iV,
4
remained there until dusk, and then emerged into the exposed half. After 20.00 hours, some of them moved back into the shaded half, the distribution of urchins in the two halves after that time being evidently random until dawn when all moved into the shaded half. Unequal distribution of food organisms or dissolved oxygen may thus be discounted as causative factors of the nocturnal migrations. The activity of the captive urchins differs from that of the natural population only in the return of some of the animals to the shade after 20.00 hours. This may be the result of random movement in a confined space, which would not occur in the natural population. Diurnal changes in food distribution, dissolved oxygen, current speed and temperature, as well as some inherent rhythm, may equally well account for the results shown in Tables I and II. Further experiments were thus designed to establish the relative importance of change in light intensity and any of these, as causative factors. Six urchins were kept in each of four fully exposed baskets until midnight when one half of each basket was shaded, the urchins being in the exposed halves. In two baskets the exposed half was illuminated, the intensity of illumination being 40 foot-candles. The urchins in these baskets quickly moved out of the increased illumination into the shaded half (Table III), whereas in the controls only very few did so, and more slowly. In a similar experiment, in which six urchins were kept in each of six completely shaded baskets during
the Exposed Half of Each of Six Haft-shaded Baskets, at Intervals Throughout Two Periods of Twenty-four Hours
Local Time Noon 12.15 hrs. 14.00 16.00 17.15 17.20 17.30 18.00 20.00 22.00 24.00 02.00 04.00 05.00 05.30 06.00
08.00 10.00 Noon
17/18.xii.55 6 6 6 1 0 0
6 0
6 0
0 0 0
0 0 0
5 6 6 5 4
3 5 6 6 5
DUSK 3 2 4 6 6 6 4 6 2 3
4 0
3
1 3
2
0 4
1 0 0 0
0 0 0 0
0 0 0 0
0 0 0
0 0 0
6 0
0 0 0
0 0 0
1 4 4 5 4
2 5 6 5 0
5 2
2 3
1 0 0 0
3 4 DAWN
6 0 0 0 0
6 0 0 0 0
4 6 6
4 5 6
18/19.xii.55. 6 6 6 0 0 0 0 0 0 0 0 0 0 0 0 DUSK 3 2 4 4 5 6 6 6 6
6 0 0 0 0 1 6 6
5
4
4
2
3
4
2
3 5
4
2 1 3 4
4 2 0 2
1 3 3 1
3 2 6 5
2 5 4 3
2 4 4 2
0 0 0 0
0 0 0 0
0 0 0 0
0 0 0 0
0 0 0 0
1 0 0 0
0 0 0 0
0 0 0 0
DAWN
THORNTON: DIURNAL MIGRATIONS OF THE ECHINOID DIADEMA SETOSUM (LESKE) Table IlL Number of Dark-adapted Urchins in the Exposed Half of each of Four Half-shaded Baskets, two of which were Illuminated in the Exposed Half after Midnight
6 0 0
24.00 hrs. 00.30 ,, 01.00 ,,
Light
No Light 6 6 5 4 3 4
6 0 0
the morning, and then three baskets halfshaded and three fully exposed at midday, the urchins in the half-shaded baskets quickly moved into the shade (Table IV). Table IV. Numbers of dark-adapted Urchins in the Exposed Halves of Three Half-shaded Baskets, and in the Original Halves of Three Fully Exposed Baskets
Halfshaded 6 6 6 0 0 0
12.00 hrs. 12.30 ,, 13.00 ,,
0
0
0
Fully
exposed 6 6 6 5 3 6 3 4 3
The complementary experiment was made in which urchins were kept in direct sunlight for two hours and then six of the nine containers half-shaded. The urchins in three of the halfshaded baskets were originally in the exposed half, those in the other three were originally in the shaded half. Those animals originally in the exposed half tended to stay there, while of those originally shaded, some moved into the exposed half (Table V). D i s c u s s i o n and C o n c l u s i o n
The movement away from increased light intensity by dark-adapted animals can be induced experimentally at times other than dawn, and it is probable that in the natural conditions of Suakin lagoon change in light intensity is responsible for the movement of urchins at dawn. There is some experimental evidence of the avoidance of shade by lightadapted individuals, but the response does not
145
seem to be sufficiently well marked wholly to account for the observed nocturnal redistribution of the natural populations. However, this factormay act in combination with others, resulting in the nightly migrations. It is possible that when the light intensity is reduced the effect of other stimuli, notably hunger, is added, causing the urchins to move out into the open. In the natural population the presence of food on the sea bed would tend to keep the animals there until the light factor was reintroduced at dawn. The more marked sensitivity of dark-adapted animals has been noted by Millot in his studies on the responses of D. antillarum to changes in light intensity, both concerning the spine reflex (Millot, 1953, 1954), and movements of the whole animal (Millot, 1954). It is possible that the diurnal screening effect of superficial pigment which he postulates for this species (Millot, 1950, 1952, 1953, 1954), also occurs in D. setosum. In the West Indies, D. antillarum, while commonly found in shady situations during the day, may nevertheless occur in appreciable numbers fully exposed to tropical sunlight in a few inches of water. The behaviour of D. setosum at Suakin differs from that of D. antillarum in showing a more marked avoidance of light during the day. Professor Millot has suggested to me that D. setosum may have a more developed photosensory system or be less welt protected. It is also possible that the Suakin lagoon, where the calm shallow water covers a relatively smooth sea bed on which no shadows are cast during the day, approaches experimental conditions more closely than the West Indian habitat. The relative lack of temporarily shaded sites on the sea bed at Suakin would make gradual hght-adaptation less likely, with the result that fewer urchins would be found in exposed situations during the day. Observations on both species f r o m other areas would be of great interest.
Table V. Numbers of Light-adapted Urchins in the Exposed Halves of Six Half-shaded Baskets, and in the Original Halves of Three Fully Exposed Baskets
Half-shaded
Urchins originally 12.00 hrs. 12.30 ,, 13.00 ,,
6 5 4
exposed
6 6 5
6 6 3
Urchins originally shaded 6 6 6 3 1 2 2 2 1
Fully exposed 6 6 6
6 5 5
6 6 6
i46
THE
BRITISH
JOURNAL
OF
REFERENCES
Fox, H. M. (1924). Lunar periodicity in reproduction. Proc. roy. Soe. B., 95, 523-50. Millot, N. (1950). The sensitivity to light, reactions to shading, pigmentation, and colour change of the sea urchin, Diadema antillarum Philippi. BioL Bull., Woods Hole, 99, 329-30. Millot, N. (1952). Colour change in the echinoid, Diadema antillarum Philippi. Nature, Lond., 170, 325-6.
ANIMAL
BEHAVIOUR,
iV,
4
Millot, N. (1953). Light emission and light perception in species of Diadema. Nature, Lond., 171, 973. Millot, N. (1954). Sensitivity to light and the reactions to changes in light intensity of the echinoid Diadema antillarum Philippi. Phil. Trans. roy. Soc., B., 238, 187-220. Accepted for publication 14th February, 1956.