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Circadian rhythms of locomotor activityin Indian walking catfish, ClariasbatrachusAnil Kumar Ramteke a , Pushpa Poddar a & Atanu Kumar Pati aa School of Life Sciences, Pt. Ravishankar Shukla University ,Raipur, IndiaPublished online: 14 Apr 2009.

To cite this article: Anil Kumar Ramteke , Pushpa Poddar & Atanu Kumar Pati (2009) Circadianrhythms of locomotor activity in Indian walking catfish, Clarias batrachus , Biological RhythmResearch, 40:3, 201-209, DOI: 10.1080/09291010802069169

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Circadian rhythms of locomotor activity in Indian walking catfish,

Clarias batrachus

Anil Kumar Ramteke, Pushpa Poddar and Atanu Kumar Pati*

School of Life Sciences, Pt. Ravishankar Shukla University, Raipur, India

(Received 12 March 2008; final version received 18 March 2008)

The circadian rhythm of locomotor activity was assayed in both sexes of Clariasbatrachus using infrared sensors connected to an Angus event recorder. Circadianparameters of locomotor activity rhythm, such as rhythm-adjusted average (Mesor),amplitude (A), acrophase (Ø) and period (t), were determined in C. batrachusmaintained under LD 12:12 (I), DD, LD 12:12 (II) and LL for given number of days ineach schedule. Each individual fish was exposed to different LD schedules in the ordermentioned above. Results of this study revealed that (1) C. batrachus is nocturnal; (2) itexhibits LD-entrainment of its locomotor activity that free-runs under constantconditions; and (3) the period of its locomotor activity rhythm is independent of thefactor gender. It appears that multiple oscillators underlie the overt circadian rhythm oflocomotion in C. batrachus. This catfish is an important commercial species andunderstanding of its circadian clock might help in the optimization of its managementand pisciculture practices.

Keywords: circadian rhythm; locomotor activity; period; gender; catfish; teleost; Clariasbatrachus

Introduction

Circadian rhythms are ubiquitous, i.e., all living organisms, including cyanobacteria,exhibit about 24-h rhythms in their physiology and behavior in the absence of externaltimegivers (zeitgebers). These rhythms help the organisms to prepare themselves forperiodic and predictable events that take place in their immediate habitat. These rhythmsare also precisely timed by an endogenous circadian clock.

It is a prerequisite to select the appropriate hands of the clock to study circadianorganization in various models. Locomotor activity has been extensively used as one of theimportant tools to elucidate and analyze the underlying mechanisms of circadianorganization in both invertebrates and vertebrates (Iigo and Tabata 1996; Hurd et al.1998; Gerkema et al. 2000; Hurd and Cahill 2002; Herrero et al. 2003; Stoleru et al. 2004;Vera et al. 2005; Rosato and Kyriacou 2006). The importance of locomotor activity instudying circadian systems was emphasized long ago (Lohmann 1967).

Circadian rhythm in locomotor activity in piscine species has not yet been studied asextensively as it has been investigated in a few invertebrate species, for example,

*Corresponding author. Email: akpati19@gmail.com

Biological Rhythm Research

Vol. 40, No. 3, June 2009, 201–209

ISSN 0929-1016 print/ISSN 1744-4179 online

� 2009 Taylor & Francis

DOI: 10.1080/09291010802069169

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Drosophila and many rodent species. Further, there are very few studies on circadianorganization in teleosts (Hurd et al. 1998). There are also very limited studies on thecircadian organization of catfish species of the Indian sub-continent (Tikariha andShedpure 2002; Yadu and Shedpure 2002a, b). These authors, however, have studiedcharacteristics of circadian rhythm in air-gulping activity, but not locomotor activityrhythm, in C. batrachus, and have reported LD entrainment of this rhythm. Further, thereare limited studies on the locomotor behavior of catfish species under constant conditions(Kavaliers et al. 1981; Tabata et al. 1989; Hurd et al. 1998; Herrero et al. 2003). Circadianorganization with reference to locomotor activity of few Brazilian cave catfishes has alsobeen investigated (Trajano and Menna-Barreto 1995, 1996, 2000; Trajano et al. 2005).

In the present study we have assayed locomotor activity in C. batrachus using infraredsensors connected to an Angus event recorder. First, we have examined whether itslocomotor activity is rhythmic under LD 12:12 cycles. Second, we have studied thecharacteristics of locomotor activity rhythm of LD-acclimated C. batrachus aftertransferring them to either constant darkness (DD) or continuous light (LL). Finally,we have evaluated the effect of gender on the characteristics of locomotor activity rhythmin C. batrachus under LD 12:12, DD and LL.

Materials and methods

Procurement of fish and acclimation

Clarias batrachus, popularly known as the Indian walking catfish, is an air-breathing fishbelonging to the order Siluriformes, family Clariidae, and is widely distributed in mostparts of Asia. Live specimens of C. batrachus were procured from the local market andacclimatized to laboratory conditions in stock aquaria for 15 days. During this period,animals were exposed to natural day length (NDL) and ambient temperature. Fishes wereprovided with small pieces of goat meat/liver on alternate days and freshwater replenisheda day after each feeding.

Recording of locomotor activity

Following acclimation, fishes were divided in two groups on the basis of their gender. Inthe first group five female fishes and in the second six male fishes (body weight rangingbetween 50 and 80 g) were selected randomly. Each individual was kept in an aquarium(61631621 cm) with an elliptical swimming path. The water was filled up to one-third ofthe height of the swimming path. The locomotor activity of each test fish was recorded byusing Infrared sensors connected to an Easterline Angus Event Recorder (Model A 620 X,1-20 Pens, Voltage type). A pair of IR sensors (Rx and Tx) was positioned appropriatelyto detect the movement of fish in the elliptical swimming path. Interruption of the IRbeam activated the writing stylus on the strip chart of the Angus event recorder.Alignment of sensors was confirmed by light indicators.

Experimental protocol

Male and female fishes were housed in separate light and temperature (20–248C)controlled chrono-cubicles. The fishes of each group were first exposed to LD 12:12 (I)followed by DD, LD 12:12 (II) and LL. The duration (days) of exposure of the fishes ofeach group was different (Figures 1 and 2). Light-on (L-on) and light-off (L-off) timings ofLD 12:12 schedules were different for male and female groups (Table 1). Intensity of light

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was maintained at 150 lux in the light fraction of the LD and the LL schedules. Thedifferent light–dark cycles were regulated by a digital time switch, Paragon-RTS.29, Relay:10 A @ 230 VAC/24 VDC. Fishes were provided with pieces of goat meat/liver aftercompletion of each experimental schedule. Fresh water was replenished a day after eachfeeding. During the experiment fishes were not fed in order to remove the masking effect offeeding schedules.

Digitization of data

Double plotted actograms were constructed for each animal. The activity data of thesecond day were pasted below and on the right-hand side of the first day data and thisprocedure was continued for the entire period of the study on each schedule. Thequalitative data on the actogram were digitized, using the technique adopted by Thurmanand Broghammer (2001). Each hour on the actogram was divided into six 10-minute binsand scored for activity. To represent the sum of the activities for the entire hour, integers

Figure 1. Actogram (left panel) of one representative example of male Clarias batrachus (MCb #04) under LD 12:12 (I), DD, LD 12:12 (II) and LL. Right panel illustrates prominent periods of thelocomotor activity rhythm in the corresponding photo-regimens.

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between 1 and 7 were used. The former digit indicated that the fish was dormantduring the entire hour and the latter indicated that the fish was active at least onceduring all six 10-minute bins. The process of digitization was completed for each dayand each fish.

Data analyses

The quantitative data were analyzed for documenting a circadian rhythm in locomotoractivity (t ¼ 24 h) with the help of Cosinor rhythmometry (Nelson et al. 1979). A rhythmwas characterized by estimating three parameters, such as Mesor (M, rhythm-adjustedmean), amplitude (A, half of the difference between the highest and the lowest value ofrhythmic function), and acrophase (or peak) (Ø, timing of the highest value of therhythmic function). Rhythm detection was achieved if the null amplitude hypothesis wasrejected at p � 0.05. The acrophase is expressed in hours (h). A power spectrum methodwas also employed for detecting prominent period (t) in individual time series forlocomotor activity of the fishes kept under different light-dark schedules (de Prins et al.1985). After obtaining, M, A, Ø and t for each individual animal, group averages andstandard errors were computed for each group (Table 1). Other conventional statisticalanalysis, such as ANOVA and Duncan’s multiple-range test were used to compareaverages obtained for each rhythm parameter.

Figure 2. Actogram (left panel) of one representative example of female Clarias batrachus (FCb #05) under LD 12:12 (I), DD, LD 12:12 (II) and LL. Right panel illustrates prominent periods of thelocomotor activity rhythm in the corresponding photo-regimens.

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Table

1.

Cosinorsummary

oflocomotoractivityrhythm

infemale

(n¼

5)andmale

(n¼

6)catfish,Clariasbatrachus.

LD

Schedule

Gender

Data

points/

anim

al

Rhythm

detection

ratio*

Rhythm-adjusted

mean,M

**

Amplitude,

A**

Peak,Ø

midnightin

h**

Peak,Ø

L-off

timein

h**

Period(h),t*

*

LD

12:12(I)

Fem

ale

192

1.0

3.45+

0.34b(5)

1.02+

0.14a(5)

19.8

+0.9

a,b,c(5)

5.4

+1.1

a(4)***

24.0

+0.0

a(5)

Male

360

1.0

4.59+

0.12a(6)

1.01+

0.09a(6)

23.1

+0.3

a(6)

5.1

+0.3

a(6)

24.0

+0.0

a(6)

DD

Fem

ale

360

1.0

4.77+

0.49a(5)

0.48+

0.02b(5)

15.1

+1.3

d(4)***

–23.7

+0.3

a(5)

Male

480

1.0

4.49+

0.25a(6)

0.42+

0.04b(6)

15.2

+0.4

d(6)

–24.4

+0.3

a(6)

LD

12:12(II)

Fem

ale

192

1.0

4.58+

0.49a(5)

1.15+

0.38a(5)

18.2

+2.2

b,c,d(5)

6.1

+1.2

a(4)***

24.0

+0.0

a(5)

Male

360

0.5

3.61+

0.29b(6)

0.53+

0.13b(6)

21.5

+1.0

a,b(5)***

4.2

+1.1

a(6)

24.1

+0.6

a(6)

LL

Fem

ale

360

0.4

2.94+

0.21b(5)

0.26+

0.08b(5)

21.3

+0.9

a,b(3)***

–25.4

+0.7

a(5)

Male

480

0.3

2.69+

0.25b(6)

0.24+

0.09b(6)

17.7

+1.6

c,d(6)

–24.5

+1.2

a(6)

Light-off(L-off)timein

female

–14:00;Light-off(L-off)timein

male

–18:00;meansbearingsimilarsuperscriptedalphabetsdonotdiffer

from

each

other

statistically

significantlyatp�

0.05;*ratioofnumber

ofanim

alsshowingstatisticallysignificant24-h

rhythm

tothetotalnumber

ofanim

alsin

each

group;**values

are

mean+

1SEM;

***wherever

outliervalues

wereexcluded

whilecomputinggroupaverages

havebeenmentioned

within

theparentheses.

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Result

Locomotor activity

All fishes, irrespective of gender, were more active during the dark phase of the LD 12:12cycle as compared with that during the light phase. The daily records of locomotor activityof catfish, one male (MCb # 04) and one female (FCb # 05), chosen as representatives, aredepicted in Figures 1 and 2, respectively. However, this day–night distinction disappearedwhile they were under constant conditions, such as in DD and LL regimes (Figures 1and 2). The rhythm detection ratio dramatically declined while the fish were under LL,irrespective of gender (Table 1).

Rhythm-adjusted mean, Mesor

In female C. batrachus, the Mesor increased statistically significantly when LD-acclimatedindividuals were transferred to DD and it decreased dramatically when shifted under theLL regimen (Table 1). However, male individuals of the same species did not exhibitsimilar changes. Surprisingly, DD-acclimated males showed a decline in Mesor whenexposed under LD (II).

Amplitude

The amplitude in female C. batrachus declined significantly when LD-acclimatedindividuals were transferred to either DD or LL (Table 1). In males, amplitudesignificantly declined only when LD-acclimated individuals were shifted under DD, butnot under LL as compared with the preceding LD (II) (Table 1). Only under the secondLD spell was the amplitude of females significantly higher compared with that of themales.

Peak

The timings of peak in locomotor activity did not alter statistically significantly as afunction of gender, except under the LL, characterized by an advance shift of about fourhours noticed in the male group of C. batrachus (Table 1). In both males and females, astatistically significant phase advance was noticed, when LD-acclimated individuals weretransferred to DD (Table 1). Subsequently phase delay was noticed when they wereexposed to LD 12:12 again. However, it was statistically significant only in the case of themale group. Further, transfer from a second spell of LD 12:12 to LL resulted in astatistically significant phase advance only in the male group. However, under both theLD regimens statistically significant alteration in peak timings was not witnessed asfunction of gender, when the peaks were computed taking light-off time as the referencepoint.

Period

Prominent periods resulting from power spectrum analysis are shown in Figures 1 and 2(MCb # 04 & FCb # 05). The period of the locomotor activity rhythm remained unalteredas a function of either gender or various light–dark regimens (Table 1). A carefulobservation of the periodograms revealed that under both LD regimens the 24-h periodwas very much prominent. In general, under DD and LL apart from the circadian period

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(t ¼ 24 h) many other secondary periods were also evident in both male and femalegroups.

Discussion

In this study, the Indian walking catfish, Clarias batrachus, exposed to LD 12:12 photo-regimen exhibited 24-h rhythm in the pattern of its locomotor activity, irrespective ofgender. Activity in the scotophase of the LD cycle was several times higher than thatnoticed in the photophase. These results corroborate with those reported earlier for otherpiscine species (Kavaliers, 1981; Iigo et al. 1994; Iigo and Tabata 1996; Gerkema et al.2000). This clearly reveals that the imposed LD cycles are acting as a synchronizer oflocomotor activity rhythm in C. batrachus and that the test fish is conspicuously night-active. In this species, LD-entrained rhythm in air-gulping activity has also beendocumented (Tikariha and Shedpure 2002; Yadu and Shedpure 2002a, b), characterizedby a higher frequency of air-gulping during the dark period of the LD 12:12 schedule. Air-gulping activity characterizes a fast upward movement to gulp atmospheric air followed bya quick descent. Thus a single episode of air-gulping involves a considerable amount oflocomotor activity. The parallelism between the locomotor activity and the air-gulpingbehavior is therefore obvious. However, the observed locomotor activity rhythm in C.batrachus could be ascribed either to the masking effects of LD cycle or to the underlyingendogenous circadian oscillator of this rhythm. The latter possibility was found to be truefor C. batrachus, irrespective of gender, especially since both males and females exhibitedfree-running rhythm under DD with average periods (t) of 24.4 and 23.7 h, respectively.The corresponding values under LL were 24.5 and 25.4 h. However, the pattern of free-runs was not very precise compared with that observed in number of insect andmammalian models. At this moment it is difficult to ascertain the cause behind theobserved noisy free-runs under DD and LL in C. batrachus.

The pattern of day–night locomotor activity was similar in both male and femaleC. batrachus. The rhythm detection ratio was found to be 1.0 in both sexes in the first spellof LD cycle. When DD-acclimated males were exposed to LD 12:12, about 50% ofindividuals did not exhibit 24-h rhythm in locomotor activity. However, Hurd et al. (1998)did not notice any gender-related effects on locomotor activity pattern in zebra fish. Theobserved difference between the males and females in the second spell of LD 12:12 couldbe ascribed to the slower rate of resynchronization in few male individuals following theirtransition from DD to LD. Could it be that the re-entrainment rate in females is fasterthan in males? Further extensive studies might answer this question satisfactorily.

The rhythm detection ratio dramatically declined in both males and females under LL.The 24-h average activity and amplitude decreased considerably under LL, irrespective ofgender. The peak timing of locomotor activity advanced significantly in males comparedwith that of the females exposed under LL. The lower level of activity accompanied withsmaller amplitude is justifiable especially since C. batrachus is nocturnal. The samephenomenon has been reported for dark-active cave loach, Nemacheilus evezardi (Pati2001, 2008). The opposite of this is true for diurnal fish species that has been amplydemonstrated in zebra fish characterized by higher levels of activity in LD and LLcompared with those observed in DD (Hurd et al. 1998).

In general, in the present study we observed the following in female C. batrachus: (1)increase in levels of 24-h average activity in DD and decrease of the same in LL; (2)decrease in amplitude in both DD and LL with a sharp decline in the later; and (3) a phaseadvance in DD and phase delay in LL compared with those when they were under LD

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12:12. The male C. batrachus differed from its female counterpart in many ways: (1) thelevels of activity in DD and LL neither increased nor declined significantly; (2) amplitudedeclined only in DD; and (3) a statistically significant phase advance was witnessed both inDD and LL compared with those obtained in the respective preceding spells of LD 12:12.The gender related variability observed in the characteristics of locomotor activity rhythmin this study could not be attributed to wider inter-individual variations among the maleindividuals, because mostly variance computed for 24-h average activity and amplitude inthe group of male catfish was considerably lower compared with that observed in thefemale group. There is probably a single report on gender-related variability of thelocomotor activity rhythm in fish species (Hurd et al. 1998). They did not find manydifferences between males and females while studying activity rhythms in zebra fish, butthey discovered a significant interaction between the factors of gender and temperature. Itis difficult to explain the sex-related changes that were observed in the present study due tothe paucity of comparable and related literature.

The average of the period of locomotor activity rhythm in C. batrachus neither variedas function of gender nor the lighting regimen. Nonetheless, the prominent period in eachfish under LD 12:12 was always 24 h, whereas in DD and LL we observed several othersecondary periods apart from the principal period (t ¼ 24 h). This clearly indicates thatunder constant conditions C. batarchus exhibited multi-frequency rhythms. Further, thisphenomenon appeared to be independent of the factor gender. The present findingsdefinitely support the previously reported hypothesis that favors locomotor activityrhythm in fish as an expression of weakly coupled multiple oscillators (Kavaliers 1978;Hurd et al. 1998). Perhaps this is the reason why multi-frequency rhythms were detected inboth sexes of C. batrachus when they were under DD and LL.

In conclusion, this study revealed that C. batrachus is nocturnal and exhibits LD-entrainment of its locomotor activity that free-runs under constant conditions. The periodof its locomotor activity rhythm is independent of the factor gender and that multipleoscillators underlie its overt circadian rhythm in locomotion. Clarias batrachus is animportant commercial species and understanding of its circadian clock might help in theoptimization of its management and pisciculture practices.

Acknowledgements

Supported by generous grants from the University Grants Commission (UGC), New Delhi, under itsDRS Special Assistance Program sanctioned to the School of Life Sciences, Pt. Ravishankar ShuklaUniversity, Raipur, India. One of us (AR) is the recipient of the Junior Research Fellowship (NET-JRF) from CSIR-UGC, New Delhi. We are thankful to Dr. Arti Parganiha, who read the draftversion of this paper and offered useful suggestions. We are grateful to the Head of the Department,School of Life Sciences, who provided us with all the essential laboratory facilities for this work.

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