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Behauioural Processes, 2 (1977) 373-382 o Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands

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Short Communication PHOTOPERIODIC CONTROL OF HIBERNATION (GASTROPODA: PULMONATA) IN HELIX POMAZIA L.

LEIF LAU JEPPESEN Zoological Laboratory, Universitetsparken 15, DK-2100 Copenhagen EJ (Denmark)

(Received 7 April 1977; revised 25 October 1977)

ABSTRACT Jeppesen, L.L., 1977. Photoperiodic control of hibernation in Helix pomatia L. (Gastropoda: Pulmonata). Behav. Processes, 2: 373-382. Different groups of Helix pomatia were exposed to short light pulses (1 or 2 hours) during a long dark period (16 or 14 hours) of a 24-hour cycle of light and dark. The effect of the light pulses on the hibernation of the snails was shown to depend on the circadian time the pulses were introduced. Some of these light pulses reduced the hibernation. In other experiments groups of snails were exposed to la-hour cycles or 24-hour cycles of equal periods of light and dark. Hibernation was reduced by the former as compared to the latter. These results show that Helix pomatia exhibits photoperiodic control of hibernation by a discontinuous or cyclic mechanism of time measurement.

INTRODUCTION

Seasonal events, such as migrati6n, aestivation, hibernation and seasonal reproduction, are behavioural adaptations to seasonal changes in environmental conditions. Such events may be controlled directly by the seasonal condition they are designed to meet, e.g. cold torpor controlled by cold; but often the events must be controlled inanother way, because they have to be initiated before the change in the appropriate environmental factor takes place; food hoarding and fat deposition have, for instance, to be initiated before snow and cold weather make feeding impossible. Ability to initiate seasonal behaviour in advance of seasonal demands pre supposes information about intervals of time, e.g. interval since last performance of the behaviour in question, or information about time of year. Information about time of year may be provided by day length, which is commonly used to time seasonal behaviour, and is especially evident in the photoperiodic time measurement which controls, at least partially, seasonal migration and reproduction in birds and diapause and polymorphism in insects (e.g. Wolfson, 1965; Lees, 1971). Information about time of year may also be provided independently of photoperiodic time measurement, e.g. by endo-

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genous circannual rhythms. Hibernation of the ground squirrel, Citellus lateral& is controlled by a circannual rhythm. The hibernation of this species was repeated for years at circannual intervals in a constant environment (Pengelly and Asmundson, 1972). It will appear from the following that hibernation in Helix is controlled partly by the cold, which it is designed to meet, and partly by photoperiodic time measurement. Information about the interval since emergence has some significance to the hibernation. Experiments on the possible participation of a circannual rhythmicity have not been performed on Helix. The main biological demand connected with hibernation in Helix pomatia is protection against low temperature. Reduced water content, increased freezing-point depression of the blood (Meyer and Thibaudet, 1937) and several behavioural adaptations serve to fulfil this demand. Prior to the inactive phase of hibernation Helix finds an appropriate place, digs a hole in the ground, turns around in the hole, forms a cover over the hole and forms a calcareous epiphragm over the shell aperture (Lind, 1968). The onset and duration of hibernation in Helix is controlled by external factors, such as temperature and humidity (Gaspard, 1823; Bellion, 1909; Fischer, 1931; Tischler, 1974), which have a direct significance on the activity of the snail. Recently it was shown that hibernation is also controlled by the photoperiod, since long days prevent or postpone hibernation (Jeppesen and Nyg&.rd, 1976). This was shown by exposing groups of snails to daily photoperiods of different lengths. Internal factors, independent of photoperiodic time measurement, may be controlling, since it takes much more time to induce hibernation in spring, shortly after emergence, as compared to summer and autumn. This was shown by Jeppesen and Nyg%d (1976), who suggested the existence of a photorefractory state following hibernation and lasting for about one month (until mid-May in the case cited). The purpose of the experiments reported here is to examine the reaction of the snails to conditions that differ with respect to the distribution of the daily periods of light and dark without differing with respect to the total length of these periods, i.e. the combined length of one or more periods of light or dark within each 24-hour cycle. The results of these experiments may strengthen the evidence that a photoperiodism, comparable to that of birds and insects, is exhibited by this mollusc species, and they may throw some light on the mechanism of time measurement.
METHODS

Adult individuals of Helix pomatia L. were collected from the wild and kept for less than a week in the laboratory at long day conditions (LD 18 : 6) and 22 C constant temperature until use. Before and during the experiments the snails were housed as described previously (Jeppesen and Nyg%rd, 1976). Light intensities were 300-400 lux during light periods and less than 1 millilux during dark periods.

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Two types of experiments were performed. The effect of 24-hour cycles of equal periods of light and dark (LD 12 : 12) was compared to the effect of 12hour cycles (LD 6 : 6), and the effect of short light pulses, which were arranged so that they scanned through a long (hibernation inducing) dark period, was assessed. Six light pulses of one or two hours duration were used in these experiments. A total of seven experiments were performed. The experimental conditions of the different experiments are given in Table I and Fig.2. Most of the behavioural measures of initiated hibernation (digging a hole, turning around, etc.) were observed. Usually the different measures were ob served in a regular succession within a few weeks, and therefore it was decided to report here only the last one: formation of a complete epiphragm over the shell aperture.
RESULTS

Comparisons between those experiments that differ with respect to starting date only, show that the earlier the starting date the longer latency of hibernation (experiment II compared to I and III, P < 0.001, Kruskal-Wallis test, two-tailed; experiment V compared to VI, P < 0.001, Mann-Whitney two-~ tailed test). The number of hibernating snails was greater in the experiments started mid August as compared to earlier (June) or later (October) starting dates (experiment I compared to II and III, P < 0.001, Kruskal-Wallis test, two tailed; experiment VI compared to V, P < 0.001, Mann-Whitney U test, two tailed). Comparisons between experiments with approximately the same starting date and the same light/dark conditions but different experimental temperatures do not permit clear conclusions concerning the effect of temperatures. The main purpose of the different experiments was to compare the reactions of the groups of snails within each experiment. The comparisons of short versus long cycles show that short cycles (6L6D) reduced the number of hibernating snails in the experiments started in August (I) and September (IV). This effect of the short cycles was not seen in the experiments started in June (II) and October (III). The mean duration of hibernation was also reduced by the short cycles. This holds true for the experiments which were started in August and June, but not for the one which was started in October. Duration of hibernation was not measured in experiment IV (Table I, Fig. 1). There was no intergroup difference in the night interruption experiment which was started in June (experiment V), but the light pulses significantly affected the hibernation (Table I) in the experiments which were started in August (experiments VI and VII). In experiment VI the hibernation was, most likely, affected in a bimodal manner, since the group in which the interruption was placed in the middle of the night (group 4), showed reduced duration of hibernation (P< 0.05, median test, one tailed) and reduced number of hibernating snails (P< 0.02, x2-test, one tailed) as compared to the re. maining groups. The significant effect of the conditions of experiment VII is

TABLE I 0 -1

Course and results of experiments I-VII Results Date Temperature ( C) No. of snails Hibernating snails Mean duration of hibernation p** Days P** 0.025 69 68 93 96 46 65 0.01 30 30 8 3 20 20 20 20 20 20 13 12 14 10 12 11 126 130 118 131 119 125 59 70 88 83 82 94 12 22 77 85 52 87 0.01 15 14 16 14 15 15 10 2 5 3 66 61 7 9 46 71 Mean latency of hibernation P* 0.05 15 14 16 14 11 14 Days

Course of experiments

No. of exp. and group L D No. 14 16

L:D

Light pulse

(Dawn at 08)

(Duration (h)) and

start

6:6 12:12

18.08.76 to 25.04.77 14.06.76 to 11.01.77 -04.10.76 to 14.03.77 12.09.75 to 12.12.75 04.06.76 to 12.04.77

II

1 2

6:6 12:12

III

1 2

6:6 12:12

IV

1 2

6:6 12:12

8:16

(1) 17 19 21 23 01 03

VI 20 20 20 20 20 20 16 15 15 15 15 15 15 5 7 9 5 7 12 57 62 85 76 78 68 14 0.05 0.05 20.08.75 to 20.12.75 19 16 19 14 20 17 78 74 84 77 83 80 143 107 115 82 112 97

1 2 3 4 5 6

8:16

(1) 17 19 21 23 01 03

0.02

0.02

18.08.76 to 23.05.77

VII

1 2 3 4 5 6

10:14

(2) 19 21 23 01 03 05

*Fisher-test/xl-test, one tailed. **Mann-Whitney U-test/Kruskai-Wailis test, one tailed. Probabilities shown in the table relate to the intergroup variation of each experiment.

less easily interpreted, although a bimodal effect on latency of hibernation seems probable (latency prolonged by interruptions placed in the middle of the dark period, see Fig.2). Duration of hibernation was not measured in experiment VII.
DISCUSSION

Jeppesen and Nyg%rd (1976) found that hibernation was performed by fewer snails and with a longer latency at photoperiods of 16 and 18 hours, as compared to phot.operiods of 12, 8 and 6 hours. They concluded that Helix pomatia exhibits photoperiodic control of hibernation. The finding of the present experiments, i.e. that hibernation depends on the distribution of daily periods of light and dark, confirms this conclusion. This is the first example of photoperiodism in the mollusc phylum. The use of day length to time hibernation is especially demanded if hibernation has to be initiated or prepared a long time before the beginning of the unfavourable conditions it is designed to meet, and this is in fact the case for the hibernation of Helix. Pollard (1975) has shown that individual snails disperse from a hibernating area during the summer and return to the same area
HIBERHATING I PERCEWlAGtI 100 A 10.. 60 -. Lb 20.. FT., 50 60.~ LO -. 20~~ 50 LO .20.. EXP m START 6110 100 150 200 OAVS EXP n HART lb/6 : ..i , , 100 I 150 ,-,:, 200 DAYS , EXP I START 18/E n _ I ., : : HAILS

: ..

...

50 10 EXP II START 1219

100

150

200

OAVS

t::::~::;:::::::;;::::::

.,...... .... :
50

:_...:
100 OAVS FOLLOWING START OF EXPERIMENT

Fig.1. Cumulated and real percentage of hibernating snails in days following the beginning of experiments I, II, III and IV.

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during the autumn, well in advance of the low temperature, from which the snails have to protect themselves. A longer period of preparatory metabolic changes may also be necessary, although clear experimental evidence is lacking (Hunter, 1964). Snails collected from the wild in autumn may be induced to hibernate within a few days by exposure to low temperature, -4 C for 4 hours (Fischer, 1931; Lind, 1968). Fischer also found that it is not possible to induce hibernation by low temperature in summer, and Lind (1968) as well as Kuhn (1914) observed
TIME GROUPIIO 06 12 16 20 _ 00 OL 08 HOURS 08 12 I 16 20 , 00 OL on

HIEEPNAIIYG

SNAILS

CUMULATED

..

REAL

NUMBER

L+ 100

L
110 200 160 100 160 200 210

LlAVS +

100

Fig. 2. Course of experiments V, VI and VII, and cumulated snails in days following the beginning of the experiments.

and real number

of hibernating

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that even if the snails are not exposed to cold they will still begin to hibernate later in the autumn. This changing reactivity to low temperatures was suggested by Fischer (1931 and Kuhn (1914) as being due to an innate annual cycle of physiological changes. It may, however, also depend on physiological changes induced by photoperiods, i.e. snails may be able to react to a low temperature if they are prepared by exposure to the short day lengths (less than 16 hours) of the late summer for a given length of time. This last explanation is suggested by the knowledge that photoperiodism does exist in Helix, and especially by the finding that hibernation was prevented throughout the autumn (end of experiment: January) in some of the long day groups (photoperiod: 18 hours; temperature: 12 C) of Jeppesen and Nyg%rd (1976). The snails reaction to the present experimental conditions did also depend on the time of year. The latency of hibernation was shorter in experiments started in the autumn as compared to those started earlier in the year. It seems likely that a photoperiodically induced preparation for hibernation might be a cause of the changing reactivity to these conditions too. According to the external coincidence model (Pittendrigh, 1972) photoperiodic time measurement is mediated by a circadian rhythm of photosensitivity. Light has two functions in this model. In its role as zeitgeber light first entrains a circadian photosensitivity rhythm. The second function of light is induction of a photoperiodic response. Dawn may set a photosensitive phase to occur and if light is present during this phase photoinduction takes place. Animals need not experience light continuously for effective photoperiodic time measurement. This external coincidence model is readiiy applicable to the present results, which show that the mechanism by which Helix distinguishes between a short day and a long day is cyclic or discontinuous. The light conditions at different times of day (or night) do not have the same significance. If it is assumed that long days induce activity in Helix, then the interval between the entraining light and the inducing light of the model has to be about 16-18 hours in order to fit the observations of Jeppesen and Nyg&d (1976): who found that daily photoperiods of 16 and 18 hours counteracted hibernation (induced activity). Such an interval between successive periods of light occurred in the present experiments in the short cycle groups of experiments I-IV, in group 4 of experiments V and VI and groups 3 and 4 of experiment VII (see Fig.2 and Table I, time of light pulse; e.g. experiment VI, group. 4: interval from main light on to light pulse off: 16 hours, interval from light pulse on to main light off: 17 hours), and it was mainly in these groups that hibernation was found to be reduced. The snails of all the rest of the groups had the possibility to seek out within each 24-hour cycle an interval between light-on and light-off which was 15 hours or less (Fig.2 and Table I. It is a common expe-ience from this sort of experiment that hour-long light pulses placed in the last part of the dark period entrain the rhythm of photosensitivity, e.g. Murton and Westwood, 1975).

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The possibility, that Helix exhibits photoperiodic time measurement as proposed by the external coincidence model, is supported by the fact that the basis of this model, a circadian rhythmicity, has been found in land pulmonates (Kratochvil, 1976) and commonly among gastropods (e.g. Stephens et al., 1953; Zann, 1973). However, the results may also be explained by an hour glass model similar to that of Lees (1971), by the internal coincidence model of Pittendrigh (1972), and by a possible non-clock influence from the experimental conditions (Pittendrigh, 1972). Further experiments are needed to evaluate the resemblance of these different models and the mechanism of time measurement in Helix.

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Stephens, G.C., Sandeen, M.I. and Webb, H.M., 1953. A persistent tidal rhythm of activity in the mud snail, Nassa obsolete. Biol. Bull., 117: 635. Tischler, W., 1974. Aussenfaktoren als AuslSser tageszeitlichen Verhaltens und begrenzter Dormanz bei Helix pomotia L. Zool. Anz., Jena, 193: 251-255. Wolfson, A., 1965. Circadian rhythm and the photoperiodic regulation of the annual reproductive cycle in birds. In: J. Aschoff (Editor), Circadian Clocks. North-Holland Publishing Company, Amsterdam, pp. 370-378. Zann, L.P., 1973. Interactions of the circadian and circatidal rhythms of the littoral gastropod Melanerita atramentosa Reeve. J. Exp. Mar. Biol. Ecol., 11: 249-261.