Effects of Light and Food as Zeitgebers on Locomotor Activity Rhythms in the Loach, Misgurnus anguillicaudatus

7 Pages·1994·8.8 MB·English

by  Mayumi Naruse

ZOOLOGICAL SCIENCE 11: 113-119 (1994) 1994Zoological SocietyofJapan
Effects of Light and Food as Zeitgebers on Locomotor Activity
Rhythms in the Loach, Misgurnus anguillicaudatus
Mayumi Naruse1* and Tadashi Oishi2
1Division ofHuman Life and Environmental Science, Graduate School of
Human Culture, and 2Department ofBiology, Faculty ofScience,
Nara Women's University, Nara 630, Japan
—
ABSTRACT Fourexperimentswereperformedtoexaminethesynchronizingeffectsoflightandfoodonthelocomotor
activityrhythminthe loach(Misgurnusanguillicaudatus). InExp. 1,foodwasgivenonceadayatthescheduledtimein
the middle oflight (L) ordark (D) phase under LD 12:12. When the fish were fed in the L phase, they showed three
types of activity pattern (light-active, dark-active and light-dark-active). On the other hand, most of the fish became
dark-activewhentheywerefedintheDphase. Inbothconditions,thefishwereentrainedwelltothescheduledfeeding.
In Exp. 2, the scheduled feeding cycle was removed from the previous Exp. 1. Under these conditions, the loach
remainedtoshowthe samepattern asthat inExp. 1 ortendedto becomedark-active. The feeding-anticipatoryactivity
peak gradually disappeared during these experiments. In Exp. 3, the fish were exposed to the scheduled feeding and
constant darkness (DD). Since almostallfishwereentrainedtothescheduledfeeding, scheduledfeedingaswell as LD
cycles is effective as a zeitgeber for the locomotor activity rhythm in the loach. Under constant conditions (Fig. 4),
free-runningrhythmswere observed, although the duration ofthe rhythm was short and the ratio ofthe individuals that
showedfree-runningrhythmswaslow(7-50%). Therefore,thelocomotoractivityrhythmintheloachisanendogenous
rhythm but the couplingbetween the oscillatorand the locomotoractivity seemsto be weak and different dependingon
individuals.
INTRODUCTION The loach (Misgurnus anguillicaudatus) is one of the
common freshwater fishes in Japan and inhabits paddy fields
One of the characteristics of the circadian rhythms in and small streams. Although there are several studies con-
fishes is variability of the rhythms compared with those in cerning the spawning behavior and season in the loach [19,
higher vertebrates [15]. The appearance of the circadian 23], thereisonlyonereportbyYanagishimaandMori [30]on
rhythmsvaries inter- [24] and intra-specifically [5, 7, 27], and the locomotor activity rhythm of the loach. They reported
even intra-individually [12]. Activity patterns showed diur- that the fish showed the exogenously controlled nocturnal
nal, nocturnal, crepuscularandintermediatetypesdepending activity rhythm because the rhythmicity immediately dis-
on fishes [24]. In the perch (Percafluviatilis) juvenile fish appeared under a constant condition. In this paper, we
,
showedanocturnal activitypatternbutadultfishchangedthe investigated (1) effects of single environmental factor, light
activity pattern to diurnal [7]. Several activity patterns (LD cycle) orfood (scheduledfeeding cycle), on thelocomo-
appeared simultaneously such as diurnal and nocturnalin the tor activity rhythm, (2) effects of the phase relationship
juvenile pink salmon (Oncorhynchus gorbuscha) [5] and between two environmental factors, light and food, on the
diurnal, nocturnal, light-change-active and arrhythmic in the rhythm, and (3)whetherthelocomotoractivityrhythmofthe
medaka (Oryzias latipes) [27]. Locomotor activity changes loach is an endogenous circadian rhythm or not.
seasonally in the minnow (Phoxinus phoxinus), the sculpin
(Cottuspoecilopus) and the burbot (Lota lota) [12], and the MATERIALS AND METHODS
medaka [31]. These reports suggest that a plastic reactivity
to various zeitgebers may induce the variability of the Adultloaches (Misgurnusanguillicaudatus) includingmales and
rhythm. Inorderto clarify thisprobability, we selected two females of about 9-16cm in total length were used. We caught
environmental factors, light and food. Light is a major them at asmallstreamalongthepaddyfieldsin KyotoPrefecture in
environmentalfactorasazeitgeberinfishesaswellasinother May, 1988, or obtained cultured fish in the Shikoku districts from a
organisms. Food has been reported to act as a zeitgeber in fish shop in April to October, 1987.
some fishes, such as the goldfish (Carassius auratus) [14] and Thefishwerekeptindividuallyinaplasticwatertank(31.5X17
the medaka [29]. cxh2a1mHbecrm)atwi2t5h+sla°nCd aatt tlheeastbototnoem maonndthplabceefdorien aexbpieorcilmiemnattsi.c
Fluorescent lamps (40W) were used as the light source. Light
intensities at the water surface were measured by a radiometer
Accepted October 15, 1993
Received July27, 1993 (UDT161, United Detector Technology Inc., California) and ad-
* Present address: Department of Hygiene, Akita University justedat460-600lux(0.26-0.39mW/cm2)or5lux(0.002mW/cm2)
School ofMedicine, Akita 010, Japan inthelight(L)phaseand luxinthedark(D)phase. Wefedabout
2 To whom reprint requests should be addressed. 0.5-1.0g wet weight of live tubifexes as food by hand or an auto
114 M. Naruse and T. Oishi
feedinginstrument(SP-10A, Nippon Denshi Kagaku, Kyoto)during RESULTS
scheduledfeedingexperiments. Tubifexeswithwaterwereputina
small plastic tube and thrown into a water tank by overturning this Experiment1 Locomotor activity rhythms under LD cycles
tubeatthefeedingtime. Asacontrol,wegaveonlywaterusingthe and scheduled feeding.
tubefor3daysjustafterthescheduledfeedingexperiment,butnone (A) Food was given at the scheduled time (12:00) in
ofthe fish reacted tothissham-feedingregimen. Waterwasalways the middle of the L phase under LD 12 12.
aerated and filtered. The locomotor activity of the loach was :
measured by a pair ofinfrared photocells (JU-33P, -33R or PL3-E, The locomotor activityLoDf the loach was classified into four
-FL, Hokuyo Denki, Osaka) at both sides of the water tank. The patterns in relation to cycle, i.e., dark-active (nocturnal)
light source and receiverofphotocellswere set at about 1cm above (ex. Fig. lA-a, B), light-dark-active(ex. Fig. lA-b,candFig.
the sand, since the loach is a benthic fish. Main activity including 2a), light-active (diurnal) (ex. Fig. lA-d) and arrhythmic.
searching and feeding behavior and most swimming behavior was The term "light-dark-active" denotes that there are peaks of
observed at thebottom layer(see the resultsofExp. 3). Whenthe activityin both L and D phases. Among 20 fish used in this
fish interrupted the beam, it was recorded by an actograph (Fuji experiment, one fish was dark-active, 12 were light-dark-
Denki, Tokyo) and the number ofinterruptions were counted by a active and seven were light-active, and the difference was
digitaldatarecorder(DDR3010, SanyoDenki, Osaka). Datafrom statistically significant (P<0.05, *2-test for one sample)
theactographwereusedforvisualexamination, andtotalcountsper (Table la). It took at least 3-5 days for the loaches to
one hour from the digital data recorder were used for the statistical
establish the stable locomotor activity pattern (see Fig. 2a).
analyses such as z2-test and periodogram analysis. In these analy-
ses, the significance level we adopted was 95% confidence limit. Fouroutofsix light-active fishtendedto change theiractivity
Inthepresentstudy,weselectedfourexperimentalconditionsto patterns from dark- to light-active during this experiment.
examine the synchronizing effects of light-dark (LD) cycles and All fish excluding one dark-active fish (Fig. lA-a) were
scheduled feeding in the locomotor activity rhythm ofthe loach and entrained to scheduled feeding (P<0.01, j2-test for one
compared the results individuallybyusingthesame membersoffish sample), and the activity was classified into two types as
throughout these experiments. Before each experiment, loaches follows. Type 1 (Ei): the peak of activity lasted several
weresubjectedtoconstantdarkness(DD)withoutfoodforatleast10 hours before the feeding time, which probably reflects the
days to eliminate the after-effect ofthe previous condition. anticipation for food (n=ll), and among these 11 fish, eight
Experiment 1 Locomotor activity rhythms under LD cycles and remained inactive for several hours after feeding (ex. Fig.
scheduled feeding.
lA-b) andthreecontinuedtobe active forseveral hoursafter
4t(h6Ae0)-L6p0Fh0oaolsudex,wuanDsd=e0gri1vLueDxn)a1t2fto:hr1e21s0(cL:(hne0d=6ul6:)0ed0o-rt1i81m5e:0((0n1,2=D::10401))8di:an0y0st.-he06mi:0d0d;leL=of flaesetdeidngse(veexr.alFihg.oulrAs-d)af.terTytphee f2ee(dEin2)g: ttihmeeacwtiitvhitoyutpetahke
t(hBe)DFpohoadsewausndgeirvernevaetrtsheedsLcDhed12ul:e1d2t(iLm:e1(81:20:00-00)6i:n00t,heDm:i0d6dl:e00o-f ranetgiicmiepnatowrayspreeapkea(tne=d8a)ft(eerx.ExFpi.g.2l-AA-c)u.singWhtheensEaxmpe.in1d-iA-
18:00) for 12 (n=6) or 15 (n=14) days. viduals, a similar tendency of activity patterns was observed
Experiment 2 Effects of LD cycles on the locomotor activity for both LD cycle and scheduled feeding.
rhythms without food after Exp. 1. (B) Food was given at the scheduled time (12:00) in
(A) Fish (n=6) were placed under LD 12:12 without food after the middle ofthe D phase under LD 12 12.
:
Exp. 1-A for 10 days. In this experiment, all fish except one light-dark-active fish
(B) Fish (n=6) were placed under LD 12:12 without food after showed a dark-active pattern (ex. Fig. IB and Fig. 2b) (P<
Exp. 1-B for 10 days. 0.01, j2-test for one sample) (Table la). A tendency to-
Experiment3 Effectsofscheduledfeedingonthelocomotoractivity
ward the change of activity pattern from light- to dark-active
rhythms under constant darkness (DD).
Fish (n=6)werefedonce adayatthescheduledtime (12:00) under was observed in four dark-active fish during this experiment.
DD (D= lux) for 11 days. Inorderto analyzethebehaviorofthe All of the 19 dark-active fish were synchronous to the
loachunderthescheduledfeedingandconstantdimlight(dimLL,L scheduled feeding (P<0.01, £2-test for one sample) (Table
=5lux), we recordedthebehaviorofafemale byVTR(TVcamera; la). The two types of entrainment to scheduled feeding as
WV-1550, Matsushita Tsushin, Osaka, Time Lapse VTR; NV-720, the previous experiment were also observed in this experi-
Matsushita Denki, Osaka). ment. The number of fish for type 1 and 2 was 18 (ex. Fig.
Experiment4 Free-runningrhythmsunderconstantconditionsafter IB) and 1, respectively.
Exp. 1 and 3. When Exp. 1-A was compared with 1-B, various activity
(A) Fourteen fish were subjected to DD without food after Exp. patterns appeared under the scheduled feeding in the L
1-A for 15 days.
(1B-)B foFrou1r5tdeaeyns.fish were placed under DD without food after Exp. tphheassec,hewdhuilleedthfeeeldoiancghinbetcheamDepehxacsleus,ivaenldytdhaerkd-iafcfteirveencuenwdaesr
(C) Six fish wereplaced underDD withoutfoodafterExp. 3for 14 highly significant (P<0.01, *2-test for multiple samples)
days. (Table la). When the activity patternswere compared indi-
All experiments were performed during November, 1987 to vidually between these two conditions, three types were
September, 1988. detected in the entrainment to LD cycles; (1) fish strongly
affected by the scheduled feeding, as they tended to be
light-activewhen theywerefedin the Lphase anddark-active
i
T
Locomotor Activity Rhythms in the Loach 115
LD-Ei
L-E1
18 24
TIME OF DAY (HR)
Fig. 1. Examples oflocomotoractivityrhythmsofthe loach in Experiment 1. (A) Exp. 1-A (LD 12:12, Foodin L). (B)
Exp. 1-B (LD 12:12, FoodinD). ActivitypatternswererepresentedasD, LDandLfortheentrainmentinrelationto
LD cycles, and Ei, E2 and N for the entrainment to scheduled feeding. D: dark-active. LD: light-dark-active. L:
light-active. E^ entrainedwiththe anticipatoryactivitypeak (type 1, see text). E2: entrainedwithouttheanticipatory
peak (type 2, see text). N: not entrained. Horizontal bar: light condition (LD 12:12, white bar: L, dotted bar: D).
Triangle: feeding time. Data were shown as mean+standard error (SE) for 10or 12 days.
Table1. The number of individual fish for each activity pattern
(a)
LD cycle Scheduled feeding
Experiments Dark-active Lc§h,tedark~ Light-active Arrhythr Entrained Nenottrained
1-A (LD 12:12, Food in L) 1 12 7 *3—t" 19
1-B (LD 12:12, Food in D) 19 1 ** 19
2-A (LD 12:12, Food removed in L) 4 2
2-B (LD 12:12, Food removed in D) 6 —
-
3 (DD, Food at 12:00)
(b)
Constant condition
Experiments
Free-run Not free-run
4-A (after LD 12:12, Food in L) 1 13
4-B (after LD 12:12, Food in D) 4 10
4-C (after DD, Food at 12:00) 3 3
*: P<0.05, Z2-test for one sample ** P<0.01, ^2-test for one sample
t+: F<0.01, #2-test for multiple samples
116 M. Naruse and T. Oishi
when they were fed in the D phase (n=7), (2) fish affected (B) Fish were placed under LD 12:12 without food
only by LD cycles, as theywere always dark-activeirrelevant after Exp. 1-B.
to the phase offeeding (n=l), and (3) the intermediate type In this experiment, all six fish were dark-active (ex. Fig. 2b)
between types (1) and (2) (n=12). In the case of entrain- (Table la). Theyweredark-activeinthepreviousExp. 1-B.
ment to scheduled feeding, there were also three types, (1) Threeofthemdecreasedtheamountofactivityinafewdays.
fish entrained with an anticipatory activity peak (type 1) When the results of Exp. 2 was compared with that of
irrelevant to the phase of feeding (n=ll), (2) fish changed Exp. 1, in five fish that were light-dark-active under the
their activity patterns to type 1 when they were fed in the D scheduled feeding in the L phase (Exp. 1-A), four fish
phase (n=7), and (3) fish did not show the anticipatory changed their activity patterns to dark-active, and only one
activity peak (n=2). fish changed to light-active. One fish that were light-active
Experiment2 EffectsofLD cyclesonthelocomotoractivity in Exp. 1-A kept the same pattern. The difference between
rhythms without food after Exp. 1. Exp. 1-A and 2-A was highly significant (P<0.01, *2-test for
(A) Fish were placed under LD 12 12 without food multiple samples) (Table la). On the other hand, the dark-
:
after Exp. 1-A. activepatterninallofthesixfishunderthescheduledfeeding
D
In six fish observed, four were dark-active (ex. Fig. 2a) and in the phase (Exp. 1-B) was maintained in the condition
two were light-active (Table la). Under LD 12:12 and the without food. Therefore, the loach is mainly a nocturnal
scheduled feeding at the L phase in Exp. 1-A, all ofthe four species and the activity peak in the Lphase seems to depend
dark-active fish showed light-dark-active pattern, while two on the scheduled feeding in the L phase.
light-active fish were light-dark- or light-active. A signi- Experiment3 Effectsofscheduledfeedingonthelocomotor
ficant reduction in the amountofactivitywas observedinthe activity rhythms under constant darkness (DD).
two light-active fish (ex. Fig. 2a) andone dark-active fishin a Five out of six fish were considered to be entrained by
few days after the beginning of this experiment probably the scheduled feeding (Table la). They showed a peak of
because of starvation. The anticipatory activity peak anticipatory activity prior to the feeding time (type 1) (Fig.
observed before the feeding time disappeared within a few 3). The amount of activity reduced just after the feeding
days. time and increased gradually until the next feeding time.
On
LD 12:12
Food in L
(Exp. 1-A)
10- m
LD 12:12
without Food
20J
C>O
<
Q
On
LD 12:12
Food in D
(Exp. 1-B)
12-
LD 12:12
without Food
22J
12 18 24
TIME OF DAY (HR)
Fig. 2. Examplesoflocomotoractivity rhythmsofthe loach in Experiment 2(LD 12:12, without Food), (a) Exp. 2-Awas
performed after Exp. 1-A (LD 12:12, Food in L). (b) Exp. 2-B was performed after Exp. 1-B (LD 12:12, Food in D).
Horizontal bar: light condition (LD 12:12).
—
1
Locomotor Activity Rhythms in the Loach 117
We recorded and analyzed the behavior of feeding-
entrained activity pattern ofa female loach under dim LL by
aVTR. This female loach showedthe type 1 in the feeding-
<L/U) 400 entrained activity pattern. We divided the behavior of the
loach into searching and feeding behavior, and other swim-
ming behaviors. Feeding crawl specified as crawling ex-
plorationwithplowing, plowingahead andgulping (including
digandtwist)wasregardedassearchingandfeedingbehavior
[28]. From the results observed every one hour, onlyswim-
ming behavior at the upper and/or the bottom layer was
IT" 12 18 24 observed till 16:00 (two hours before the scheduled feeding
TIME OF DAY(HR) time). Searchingbehaviorandrestwere addedtoswimming
Fig.3. An example of locomotor activity rhythms of the loach in at 16:00-17:00. Swimming at the upper layer decreased
Experiment 3 (DD, Food at 12:00). Horizontal bar: light and searching behavior relatively increased, and swimming
condition (DD). Triangle: feedingtime. Datawereshown as near the place where the fish was always fed was frequently
mean+SE for 11 days.
15-
DD
without Food
30-I lIiitmiimitiiiiinmiiiiTliTi-mimiiiuiiMii11t ti1iir ii iir iii m1i1imi rirr ^F+r n—rnrrrn—rrrtittni—iiiriainiii1i1iiii—ii—i-—ii—mi 1—i1111
0-,
LD 12:12
Food in D
C/> (Exp. 1-B)
<15
Q
DD
without Food
30J i i imTfiiniinrr
DD
Food at 12:00
| (Exp. 3)
DD
without Food
25J
r~
12 24 12 24
TIME OF DAY (HR)
Fig.4. Free-running locomotor activity rhythms of the loach in Experiment 4 (DD, without Food), (a) Exp. 4-A was
pEexpr.fo1r-mBed(LafDte1r2E:x1p2.,F1o-oAd(iLnDD)1.2:12r,=F2o4o.d1hirn.L).(c)FErxepe.-r4u-nCniwnagsppeerrifoodr(mre)d=a2f3t.er5Ehxrp..3(b()DEDx,p.Fo4o-dBawtas12p:e00r)f.ormerd=a2f4t.e7r
hr. Datawere double-plotted.
'
118 M. Naruse and T. Oishi
observed at 17:00-18:00. When the food was given at (Periophthalmus cantonensis) the locomotor activity rhythm
,
18:00, the fish fed it within a few minutes and gradually could be entrained to the 12-hour feeding cycle [13]. The
became inactive. Whenever the fish was active, it was channel catfish (Ictaluruspunctatus) showed subjective feed-
usually at the bottom layer. There were swimming and rest ing time under ad-lib feeding regimen [17]. In contrast, the
at the bottomfrom 19:00 to 22:00. Swimming at the upper scheduled feeding did not affect the locomotor activity
layer appeared at 22:00-23:00 and it was increased at rhythm in the blenny {Blenniuspholis) [4].
23 00-0 00. This series of behavior corresponded to the Feeding both in the L phase and in the D phase could
: :
feeding-entrained activity pattern of the female loach re- entrain the activity rhythm of the loach (Exp. 1). The
corded by the actograph. In this experiment, it was shown activity pattern varied widely when the fish were fed in the L
that the scheduled feeding could induce the locomotor activ- phase, buttheywereconsistentlydark-activewhen theywere
ity rhythm of the loach. fedintheDphase. InExp. 2, the activitypatternstendedto
Experiment 4 Free-running rhythms under constant condi- change to dark-active under the regimen without food.
tions after Exp. 1 and 3. Therefore, fundamentally the loach seems to be a nocturnal
DD
(A) Fish were subjected to without food after Exp. species. Benthic fishes, such as the eel, catfish and loach,
1-A. havebeenconsideredasnocturnalorlight-dark-activespecies
Only one of the 14 fish showed free-running rhythms for because benthic fish approach to their food horizontally and
about 15days(r=23.5 hr) (Fig. 4a,Table lb). Thisfishwas rely on not only vision but also other senses to findfood [20].
light-active and entrained to scheduled feeding as type 1 in However, since cone cells and cone visual pigments (iodop-
the Exp. 1-A. sin-like substances) existed in the retina of the loach [11],
DD
(B) Fish were placed under without food after they seem to have an ability to be active during daytime. In
Exp. 1-B. thefield, probablytheavailabilityoffoodforthe loachdonot
Fourofthe 14fish showed free-runningrhythms for about7- change diurnally because the loach is an omnivorous detritus
13 days. One of them showed shorter free-running period feeder. In the present study, however, loaches were en-
than 24.0hr (r=22.0hr) and three fish showed longer free- trained to the daily feeding cycle, although food (tubifexes)
runningperiodsthan24.0hr(r=24.1,24.1 and25.6hr) (Fig. was not taken away, and thus, the fish could feed these
4b, Table lb). All of these fish were dark-active and en- tubifexes alive in the bottom sand whenever they want, and
trained to scheduled feeding as type 1 in the previous Exp. this was supposed to provide a weaker influence on the
1-B. entrainment than the food-removed regimen. Thus, the
DD
(C) Fish were placed under without food after importance offeeding in the circadian structure of the loach
Exp. 3. should not be neglected.
Three of the six fish showed free-running rhythms for about Davis and Bardach [3] indicated the importance of the
5-9 days. One fish showed the free-runningperiod of22.1- anticipatory activity peak that appeared prior to the sche-
23.7 hrandtwofishshowedfree-runningperiodsof24.7 (Fig. duled feeding time. This activity peak was also mentioned
4c) and28.2hr(Table lb). Thefishwith r=28.2hrshowed by Aschoff [1], in which it was suggested to appear under
free-running rhythms throughout Exp. 4-A to C. The free- both LD cycles and constant conditions. In the present
running period in Exp. 4-A and B was 23.5 and 22.0hr, study, the loach showed the anticipatory activitypeak in both
respectively. Two fish with longer free-running period than LD cycle and constant darkness (DD).
24hr were entrained to scheduled feeding as type 1 in the The loach showed conspicuous resting periods ofseveral
previous Exp. 3 and one fish with shorterfree-runningperiod hours after the feeding time. There were no reports about
than 24hr was not entrained to scheduled feeding. this type of resting period in the study of the feeding-
Since free-running rhythms were observed after entrain- entrained rhythm. Thus, this resting period may be unique
ment tothescheduledfeeding, feedingcanbeconsideredasa to the locomotoractivity rhythmofthe loach entrainedto the
zeitgeber in the loach. feeding time. The reason why the loach needs this period
maybe duetothefactthattheyare benthicfishand they have
DISCUSSION to spend many hours to digest food [26].
It has been suggested in fishes that free-running rhythms
Reports on the effect of scheduled feeding cycles on the are labile anddonot lastforalongtime [15, 18], and the ratio
locomotor activity rhythm have been increasing. In the of individuals with free-running rhythms is lower than those
goldfish (Carassius auratus), the scheduled feeding with LD of higher vertebrates, although there are some exceptions
cycle affected the locomotor activity rhythm, growth rate, such as the lake chub (Couesius plumbeus) [9], the goldfish
and serum-cortisol and -thyroxine concentrations [14, 21]. [10], two species ofthe hagfish (Eptatretus burgeri, Paramyx-
In the medaka (Oryzias latipes), scheduled feedingcycles had ineatami) [8, 16] and the catfish (Silurusasotus) [25]. In the
different influenceson the different typesofbehavior, that is, loach, free-running rhythms lasted for 5-15 days and thus,
the agonistic behaviorwas entrained to the feedingcycle, but the locomotor activity rhythm of the loach is an endogenous
the egg laying and courtship behavior were entrained rather circadian rhythm. However, the ratio of individuals which
to LD cycles than to feeding cycles [29]. In the mudskipper showed free-running rhythms was low and varied from 7 to
Locomotor Activity Rhythms in the Loach 119
50% depending on experiments, and the rhythm persisted oscillations. In "Rhythmic Activity of Fishes" Ed by JE
only for short periods. This indicates that the extent of Thorpe, Academic Press, London, pp 1-19
coupling between the oscillator and the locomotor activity 13 Nishikawa M, Ishibashi T (1975) Entrainment of the activity
seems to be weak and might differ dependingon individuals. mrhuysthcmantboynetnhseicsyc(lOesboefcfke)e.dinZgoionlthMeamgud84-:sk1i8p4p-e1r8,9Periophthal-
Since the periodic feeding in the rat caused to uncouple 14 Noeske TA, Spieler RE (1984) Circadian feeding time affects
the feeding-anticipatory peak from the component of free- growth offish. Trans Am Fish Soc 113: 540-544
running rhythm [2, 6, 22], it is suggested that the feeding- 15 Oishi T (1991) Fishes. In "Handbook of Chronobiology (In
entrained oscillator is different from the LD cycle-entrained Japanese)" Ed by Y Chiba, K Takahashi, Asakura Shoten,
oscillator. The SCN-lesioned animal that showed arrhyth- Tokyo, pp 69-78
mic locomotor activity also showed the anticipatory activity 16 Ooka-Souda S, Kabasawa H, Kinoshita S (1985) Circadian
rhythms in locomotor activity in the hagfish, Eptatretus burgeri,
prior to feeding [2, 22]. Different oscillator systems for and the effect ofreversal oflight-dark cycle. Zool Sci 2: 749-
feeding and LD cycles might also exist in the loach, because 754
the uncoupled anticipatory peak was observed and gradually 17 Randolph KN, Clemens HP (1976) Some factors influencing
disappeared in Exp. 1-A and 2-A. thefeedingbehaviorofchannelcatfishincultureponds. Trans
Am Fish Soc 105: 718-724
18 Richardson NE, McCleave JD (1974) Locomotor activity
ACKNOWLEDGMENTS rhythms of juvenile Atlantic salmon (Salmo salar) in various
light conditions. Biol Bull 147: 422-432
We are grateful to Prof. Yoshihiko Chiba, Dr. KenjiTomioka, 19 Saitou K, KatanoO, KoizumiA(1988) Movementandspawn-
Department of Biology, Yamaguchi University, and Mr. Sou ing of several freshwater fishes in temporary waters around
Miyake, Department of Electrical Engineering, Kyoto University, paddy field. Jpn J Ecol 38: 35-47
forproviding us actographs and the program ofthe actogram. 20 SawaraY (1989) The ecologyofrhythmic activityinfishes(I).
Biol Sci 41: 57-67
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