Entrainment of the circadian rhythm of food demand by infradian cycles of light-dark alternation in Hoplosternum littorale (Teleostei) Thierry Boujard, Y. Moreau, P. Luquet
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Thierry Boujard, Y. Moreau, P. Luquet. Entrainment of the circadian rhythm of food demand by infradian cycles of light-dark alternation in Hoplosternum littorale (Teleostei). Aquatic Living Re- sources, EDP Sciences, 1991, 4, pp.221-225. hal-02714622
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Entrainment of the circadian rhythm of food demand by infradian cycles of light-dark alternation in Hoplosternum littorale (Teleostei)
Thierry Roujard ('), Yanri Morcau arid Pierre Luyuct
I,VRA, Hydrubiulugie, HI' 70y, 97.787 X"OUIOII Cedex, 1;rance.
Rrceikrd April r y, I!)~)I; acccptcd July r, 1991. "' Prcscnt addrcss: I,VRL4 Hydrubioloçie, RP3, 64310 Aicain, fiarup.
Boujard T., Y. Morcau, P. Luquct. Aquat. Liring Re.~our.,1991, 4, 221-225.
Abstract Hoplosterum littorale (Hancock, 1828) shows a markcd circadian rhythm of food demand. Feeding activity is mainly nocturnal, with two pcaks, and is synchronized with the diel light cycle. We tested the cffect of infradian (period >28 h) lightldark cycles on this rhythm in fish wilh dcmand-fccdcrs: fish subjected to a 13.5 L122.5 D lightldark cycle for 8 days and a 25.5L/10.5D cycle for a further 8 days showed a strictly nocturnal fccding activity, a response that only passively reflected the cyclic altcrnation of light and dark.
Keywords : Siluriform, diel cycle, fccding rhythms.
Synchronisation du rythme circudien d'auto-distribution d'aliments par des cycles infrudiens d'kcluirugr chez Hoplostcrnum littorale (Teleostei).
Résumé Hoplosternurn littorulc (Hancock, 1828) préscntc un rythme circadien marqué d'auto-distribution de nourriture. Ce rythme, à acrophase nocturne, se caractérise par deux pics, il est synchronisé par l'alternance jourInuit de la lumière. Nous avons mis à l'épreuve Ic caractère circadien (24&4h) de ce rythme à l'aide de distributeurs d'aliments «A la demande)). Les poissons soumis à un éclairage simulant la photopériode naturelle (13.5 5110.5 N) ont un rythme circadien d'auto-distribution d'ali- ments. Lorsqu'ils sont sujets à un cycle d'éclairage infradien (période >28 h) à longue scotophase (13.5 5122.5 N) durant Sjours, puis à longue photophasc (25.5 J/10.5N) durant 8 autres jours, ils ont un cycle d'auto-distribution d'aliments qui est entraîné sans délai par les changements successifs de cycles d'éclairage, et se nourrissent exclusivement durant les scotophases.
Mots-clés : Siluriforme, rythmes circadicns, cyclcs nycthéméraux, alimentation.
INTRODUCTION alternation of day and night, or dawn, or dusk) or temperature (Randolph and Clemens, 1976). It may A circadian rhythm (24f 4 hrs.) is characterized by be endogenous, i. e., persisting with its own period in its amplitude, mean value (or Mesor) and acrophase constant environmental conditions, or exogenous if it (Gwinner, 1986; Halberg et al., 1977; Koukkari etul., only passively reflects the cyclic fluctuations of the 1987). It is generally synchronized by photoperiod (or environment. Circadian rhythms have been demon- Aquat. Living Resour. 91/04 221 05 $ 2.5010 IFREMER-Gauthier-Villars T. Roujard et al.
strated in a varicty of eukaryotes, with most applica- thereafter changcd to a 36hrs. light cycle with a tions in thc field of chronopharmacology. Spieler longcr scotophase for a period of 8 days from the 30th (1977), and later Parker (1984), suggested that such of January 1990 (13.5 L122.5 D), and subscquently to rhythms could be uscd to improve production cffici- a cycle of 36 hrs. with a longer photophase for another ency in aquaculture. period of 8 days, from the 7th of Fcbruary 1990 The feeding pcriods of fish living in natural (25.5 Ll10.5 D). environmcnts follow a marked dicl cycle (Elliott, Each tank was fittcd with a metal rod which closcd 1973; Müller, 1978; Jacob and Nair, 1983; Sagar and a 12V circuit whcn a fish moved the rod. A 220V Glova, 1988; Walsh et al., 1988). In artificial rcaring feedcr dclivcred 1 g of food via a rclay. This devicc conditions, and with the exception of Rozin and was coupled to a computcr, which recorded the hour, Mayer (1961) who found no circadian rhythm in date and tank numbcr of each demand for food. In the fccding activity of Curu.s.~iu.suurutu.s, most other order to rcstrict unintentional triggering of the feeder authors report strong circadian patterns of feeding in by thc fish, the rod was located 2cm below the water fish (Hoar, 1942; Adron etul., 1973; Hirata, 1973; surface, i.e., far from the usual zone of activity of Landless, 1976; Grove et al., 1978; Eriksson and Van this bottom dweller fish. Furthermorc, thc thank Veen, 1980; Boujard etul., 1990). Lightldark alterna- design was such that unconsumed food pellets were tion is generally thought to bc the main synchronizcr constantly drained from the thanks with the water (Gibson and Keenleysidc, 1966; Chaston, 1968; Man- ovcrflow. WC therefore know that the consumption teifel etal.. 1978; Müller, 1978; Molina Borja etul., of food could take place only within a few minutes 1990), and in CU~USS~U.~au ru tu.^, feeding rhythm is after demand-feeding. Operators entered thc cxpcr- free-running for at least 5 days (Spiclcr and Clough- imental room only cvcry 3-4 days and hcncc the fish crty, 1989). Meal times also affcct growth rates (Otta- werc disturbcd very little during the cxpcriment. way, 1978; Greenland and Gill, 1979; Nocskc et ul., 1981; Sundararaj ctul., 1982; Noeskc and Spieler, 1984; Nocske-Hallin etul., 1985), and can act as a synchronizer for several bchavioural parametcrs RESULTS (Weber and Spieler, 1987; Spieler and Cloughcrty, 1989) and for a large number of circulating hormones (Leatherland et ul., 1974; Spieler, 1977; Spieler et al., The timing of food dcmand during the threc consc- 1977; Eales et al., 1981; Spiclcr and Noeske, 1981, cutive periods with different light cycles, from the 1984; Perez etal., 1988). 22nd January to the end of the experimcnt, is shown in .figure 1. Regardless of the lighting cycle, self-feed- On the basis of thcsc observations, and with thc ing always took place throughout the phase of dark- aim of improving thc production of Hoplo.sternum ness and was infrequcnt during the light phases. littorale, a siluriform fish of economic intcrcst for French Guiana (Boujard etul., 1988), the circadian Figure2 shows the distribution of food dcmand rhythm of food intake in this species was described during the scotophases for each of thc three condi- using demand-feedcrs chccked every 3 hours (Roujard tions. When the lighting cyclc simulated the natural et al., 1990): food demand, synchronized by day-night photoperiod, food dcmand followed the same timing shifts, was characterized by a nocturnal acrophase. as that obscrved by Boujard etul., (1990), i.e., a Using the same device as in thc previous experiment, significantly bimodal feeding activity (p
Aquat. Living Resour. Feeding rhythm in Hoplosternum littorale
30101 31/01 O1 /O2 OU02 03/02 04/02 05/02 ma rml no data --- *- Li 4 - - mie; 07/02 08/02- 09/02 -10102 11/02 12/02 13/02 14/02 1 Ft IT u 10 ' -LL -m,m I 4 - no data - -
O 05 115 2 25 3 35 4 45 5 55 6 55 7 75 8 Time (days)
Figure 1. - Timing of thc sclf-distribution of food during the diffcrcnt lighting regimcs and 10r the 4 groups of IO fish studicd. Black squares indicate hours during which morc than I g was demanded, white squares indicate hours during which only 1 g was demanded. Scotophasc corresponds to the hatchcd parts oP the graph.
Table 1. - Mean amounts of self-distributcd food expressed as % of live weight pcr unit time. Total duration of the Iight/dark cycle (hrs.) 24.0 36.0 36.0 Lcngth of the scotophasc (hrs.) 10.5 10.5 22.5 ~-.- - Food-demand per hours during the scoto- phase 0.37 0.57 0.24 Food-demandi24 hrs. 3.9 4.0 3.4
Thc high variability in food demand between tanks and days was caused by moisture in the device, which happened in tank4 on 25th and 26th January, in tank2 on 2nd and 3rd Fcbruary, and in tank4 between 7th and 14th February. During these pcriods, thc fish were not able to obtain food on demand. The observed differcnces of food demand between tanks were high, especially during the last phase of the experiment. This was probably also caused by moisture in the device, making it more or less difficult for the fish of the different tanks to close the 12V line. However, if these experimental failures restrict the sienificance of the results in terms of amount of food demand, they do not affect at al1 the significance of the temporal variations of the demand.
DISCUSSION
The endogenous aspect of a diel cycle is generally tested with isolated individuals in a constant environ- ment (Millet and Manachere, 1983; Koukkari etul., 1987). In such a "free-running" situation, endogenous rhythms are revealed by their specific periodicity, each
Figure 2. - Quantity of food sclf-distributed in each series expres- individual within a given species tending to exhibit a sed in % of live weight per 1.5hrs. during: A) 24hrs. cycle; slightly different periodicity. In the case of Hoploster- 13.5 L110.5 D; tanks 1, 2, 3, 4. B) 36 hrs. cycle; 13.5 L122.5 D; num littorale, individuals isolated from their con- tanks 1, 2, 3, 4. C) 36 hrs. cycle; 25.5 Ll10.5 D; tanks 1, 2, 3. geners did not use the rod to demand food and
Vol. 4, n" 4 - 1991 224 T. Boujard et al. starved (unpublished data). Moreover, social interac- the circadian rhythm of food intake was synchronized tions appear to be important in Cullich/yidue (Kramer hy an extcrnal and periodical stimulation, the light. and Graham, 1976). In Hoplo.rtc~rnurnliltorule reared As a result, in Hoplosternurn li//orule,feeding activity in ponds, one can see air-breathing fish moving in might he an exogenous rhythm, and if not, it is only shoals of 10 to 25 individuals, swimming close to the wcakly coupled to an endogenous oscillator, with a bottom, and periodically moving up to the surface masking effect of the photophase. The strong relation- one after the other (unpublished data). ship between scotophase and fccding emphasize the In our experimcnt, in the case of an endogenous fact that this spccies is truly nocturnal, and in rearing rhythm a decrease in self-feeding was expected to be conditions, fecding the fish by night might improve observcd during late scotophase when the latter is survival or growth, but this hypothesis remains to be prolongcd, or an onxt of self-feeding was expected tcsted in ponds. Nevertheless, our results show that during late photophase when that phase is prolongcd. artificially increasing the scotophase length docs not Neither of these two responses were obtained, and increase daily food consumption.
Acknowledgements This work was funded by a grant from C;CS.BBA. Wc are grateful to J. F:. Leathcrland, D. L.G. Noakes, R. E. Spiclcr and one anonymous rcfcree for having rcad and criticizcd this manuscript, and to Kirsten Rcrat, who translated the first version of this manuscript into English.
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Vol. 4. no 4 - 1991