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Response curves and free-runningperiod of the circadian locomotorrhythm of Talitrus saltator (Crustacea:Amphipoda)Amel Ayari-Akkaria & Karima Nasri-Ammara

a Faculté des Sciences de Tunis, Unité de recherche Bio-Ecologieet Systématique Évolutive, Université de Tunis El Manar, Tunis,2092, Tunisia.Accepted author version posted online: 22 Apr 2013.Publishedonline: 25 Jun 2013.

To cite this article: Amel Ayari-Akkari & Karima Nasri-Ammar (2014) Response curves and free-running period of the circadian locomotor rhythm of Talitrus saltator (Crustacea: Amphipoda),Biological Rhythm Research, 45:2, 209-218, DOI: 10.1080/09291016.2013.797159

To link to this article: http://dx.doi.org/10.1080/09291016.2013.797159

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Response curves and free-running period of the circadian locomotorrhythm of Talitrus saltator (Crustacea: Amphipoda)

Amel Ayari-Akkari* and Karima Nasri-Ammar

Faculté des Sciences de Tunis, Unité de recherche Bio-Ecologie et Systématique Évolutive,Université de Tunis El Manar, Tunis 2092, Tunisia

(Received 3 March 2013; final version received 3 April 2013)

The amphipod, Talitrus saltator is a supralittoral species inhabits non-permanentburrows along the sandy beach. Its locomotor activity rhythm is largely studied inseveral beaches and by several authors. The present study was performed in order tobetter understand the limits of entraining of the locomotor rhythm of this species.The recording was carried in 30 specimens maintained individually, for the firstsix days in continuous darkness followed by light pulses of 3 h in constant darknessentraining all hours of the day, six days of recording separates the two successivepulses. After the experiment, the phase response curve is constructed to determinethe sensitivity of this nocturnal species to light pulses.

Keywords: phase response curve; locomotor rhythm; Talitrus saltator; Tunisia

Introduction

Talitrid amphipods constitute one of the predominant arthropod groups in sandy beachfauna exhibiting a dynamic equilibrium with environment. Owing to their ecologicalimportance, talitrids have been studied worldwide from behaviour, behavioural plasticityand genetic determination of different behaviours (Marques et al. 2003). Among thesetaltrids, Talitrus saltator, a supralittoral amphipod, has been studied as an importantmodel animal. The nature of phase control or entrainment of biological rhythm is animportant aspect of our understanding of the mechanism of biological “clocks” (Wil-liams 1980). Circadian clocks in animals regulate the timing of molecular, physiologicaland behavioural rhythms (Levine et al. 2002). Pardi and Grassi (1955) noted that thenocturnal surface locomotor activity rhythm was phase-shifted by experimentalphotoperiod suggesting that the rhythm may also be controlled by an endogenous“clock mechanism”.

The phase response curve (PRC) is universal, from unicellular to man, which differsfrom one species to another by the extent of both delay and advance phases and evenwithin the same species, it differs from one individual to another. Then, the values ofdelay and advance phases placed the limits of entraining. Furthermore, the PRC definesthe phase-dependent, qualitative and quantitative variations in the sensitivity of anendogenous rhythm over a complete circadian period, which is characteristic for a par-ticular “signal strength” of the synchroniser (Enright 1965; Chandrashekaran & Loher1969). Moreover, several types of stimulus were used to measure the response systems:

*Corresponding author. Email: ayariamel@gmail.com

Biological Rhythm Research, 2014Vol. 45, No. 2, 209–218, http://dx.doi.org/10.1080/09291016.2013.797159

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visible light pulses, ultraviolet light, vibration, temperature and chemical pulses(DeCoursey 1983).

The present study was carried to characterise the endogenous locomotor rhythm ofT. saltator under a regimen of photic pulses of 3 h, entraining successively all hours ofday. Furthermore, the PRC curves obtained from these following experiments mayexplain the phase relation between endogenous rhythm and synchroniser.

Materials and methods

Adults of T. saltator were manually collected in the morning during their above grandactivity from Bizerte beach (37° 19′N–9° 51′E) in Tunisia. The specimens were kept inplexiglas boxes with moist sand and transported immediately to the laboratory.

Thirty adult males, easily distinguished by long first antennae, were transferred indi-vidually into the actographs and kept in a controlled environment cabinet that is main-tained at a constant temperature of 18 ± .5 °C. The recording chambers consisted of anannular arena, 9.5 cm high and with inner and outer diameters of 4 and 11 cm, respec-tively. Each actograph contains a platform and was filled with moist sand, from the siteof collection, to a depth of 2 cm into which the experimental animals were able to bur-row. Food in the form of small washers of carrot was given. Locomotor activity in eachactograph was monitored photoelectrically as the frequency of interruption of aninfra-red light beam focused across the platform. Interruptions of the light-beam by theanimals caused an event to be registered on a data logger, which downloaded to twocomputers the number of interruptions of each beam as a separate channel every 20minthroughout the experiments (D.D. Green, Biosciences Workshop, University of Birming-ham, UK).

To determine PRCs for the spontaneous locomotor rhythm, the sand hoppers,T. saltator was kept firstly in free-run for six days to reveal the endogenous circadianperiod. And then, we applied light pulses of 3 h in constant darkness (DD), entrainingsuccessively all hours of day. Each pulse was applied only once and the next is appliedsix days after, in order to study the endogenous rhythms.

For better visualisation of raw data, the Chart 35 software was used to display dataas a double-plotted actogram. These data were then subjected to periodogram analysisusing the programme, TIME SERIES (Gerard Harris, Computing, Bristol, UK). Theperiod revealed was accepted as rhythmic when the periodogram peaks exceeded thethreshold of 99%. The definition of rhythm i.e. the degree to which a stronglyexpressed, clear rhythmic signal was obscured by random “noise” and was estimatedfrom the periodogram as a signal-to-noise ratio (SNR), by measuring the differencebetween the peak periodogram value and its corresponding 95% threshold limit. Thewave form curve is constructed accordingly based on the period determined for eachspecimen. Differences in the period after each pulse were calculated using the Kruskal–Wallis test.

Results

Locomotor rhythm phenology

After 55 days of the experiment, the mortality rate was equal to 57% (17/30 specimens).Thus, the determination of the circadian rhythmicity revealed 28 rhythmic individualsfrom a total of 30.

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Raw data were displayed as a double-plotted actogram by the software Chart 35(D.D. Green, Biosciences Workshop, University of Birmingham), showing cumulativeactivity values per 20-min intervals. This provided the option of normalising the databy expressing each locomotor value as a percentage of the highest value for the 24 hover which it occurred or the highest value over the entire time series; (Cummings &Morgan 2001). The analyses of these actograms allowed us to sub-divide them intothree groups. The most representative actogram of each group was represented in Fig-ure 1. The locomotor pattern obtained in Figure 1(A) was observed in 15 individuals ofT. saltator among the 28 rhythmic individuals. After the application of the pulse (a),during J1–J6, a drift to the right is observed in the middle of the subjective day: the ani-mal anticipates every day their locomotor activity. The pulses (b) and (c) applied duringthe late subjective day and late subjective day/early subjective night, have the sameeffect; in fact, a phase advance is observed during days J14–J16 and J21–J23, while theactivity is started later day-after-day during J17–J20 and J24–J27. This phase delaycontinues even after the application of the pulse (d) at the beginning of the subjectivenight until the application of pulse (e) in the middle of the subjective night, whichcaused a phase advance during the next six days. The application of pulse (f) in the endof the subjective day caused a phase advance for both days, J43–J44 and this responseis followed by a drift of locomotor activity in the left and continues until the end of theexperience even after the application of the pulse (g) at the beginning of the subjectiveday.

The Figure 1(B) was recorded in 6/28 specimens. The locomotor activity drifted tothe right during the first six days of continuous darkness. However, after applying thefirst light pulse (a), an escape phenomenon of the locomotor activity rhythm isobserved. After the second pulse (b), rhythmic activity restarted with phase delay duringJ14–J20. The application of pulse (c) placed between 18 and 21 h (late subjective day/early subjective night), caused a shift right of locomotor activity at J22–J25 so that inJ26, the drift is reversed to the left. The application of the pulse (d) has led to a phaseadvance again during the J27–J30 followed by a phase delay until the application of thepulse (e), this last, placed in the middle of the subjective night, caused a phase advanceduring the following days. After two days of applying pulse (f), we observed the recov-ery of the escape phenomenon of the rhythm until the end of the experiment.

The 3rd type of profile shown in Figure 1(C) revealed the locomotor activity of 7/28 individuals. T. saltator (7/28 individuals) started their locomotor activity later duringthe first three days of continuous darkness. During the J4–J7, a phase advance isobserved and persisted even after applying the pulse (a) placed between 12 h and 15 hof the subjective day. From J8, locomotor activity drifted to the left and persisted untilJ19. The application of pulses (c) and (d) is followed by a some response we observeda phase advance for three days, whereas, from J23 to J30, the rhythmic activity derivedto the left and the drift persisted even after applying the pulse light (e). On 41th day,we applied the light pulse (f), which caused a phase advance to the 45th day. From the46th day, the individuals of T. saltator were arrhythmics: the escape phenomenon of thelocomotor rhythm is installed.

During the first six days of free-running and days after each light pulse, we havecarried out a waveform curve. The analysis of different actograms and waveformsshowed the presence of three different patterns of activity: unimodal, bimodal and mul-timodal.

Figure 2 shows that under the first six days of continuous darkness, the specimensof T. saltator are characterised by the presence of the three types of patterns with

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similar percentages. However, after the seventh pulse, the bimodal pattern disappearedcompletely while the multimodal pattern became the dominant (85%); which can beexplained by the escape phenomenon observed at the end of the experiment.

(A)

10H30

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Hours

(B)

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21-00

03-06

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18-21

Hours

Figure 1. Double-plotted actogram of the circadian locomotor rhythm in T. saltator under thePRC experiment. The symbol 12-15 indicates the duration and the day of pulse, the bars abovethe actogram indicate the time of application of pulse (3 h). (a) 12 h–15 h; (b) 15 h–18 h; (c) 18 h–21 h; (d) 21 h–00 h; (e) 00 h–03 h; (f) 03 h–06 h et; (g) 06 h–09 h.

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Locomotor activity rhythm parameters

Results showed that T. saltator, throughout the experiment of phase response, hasmaintained a circadian periodicity with an ultradian component of about 12 h(Table 1). The statistical test of Kruskal–Wallis did not reveal significant differencesbetween both circadian (p= .6451) and ultradian (p= .4756) periods during days aftereach pulse (Table 1). Moreover, the shortest period was recorded during the firstsix days of experience. In addition, the SNR values showed that the circadianrhythm was defined better than the ultradian one (Table 1). According to Figure 3,corresponding to the variation of means of circadian periods and their SNR values,we noted that when the period is more close to 24 h, the stability of the locomotorrhythm was defined better. Figure 4, representing the dependence of the ratio activ-ity time (α)/rest time (ρ) on the circadian period, shows a positive correlation: thelonger the period, the higher the activity time. Furthermore, the longest period wasrecorded at the end of the experiment after the application of both the sixth andseventh light pulses (Table 1).

The PRCs

The intra-specific variability of PRC was revealed on individuals of T. saltator (Fig-ure 5); thus, all curves (PRC) have the same sinusoidal aspect (Figure 5). Referring toendogenous periods recorded at the beginning of the experiment, the phase advanceswere brought up while the phase delays down.

To obtain more objective interpretation of the CRP, we choose an example typeamong the specimens of T. saltator tested. On the Figure 6B, the endogenous perioddetermined during the first six days of free running is equal to τ24/DD = 24 h 40′. Afterapplying the first, second and third pulses, this period became more and more shortsubsequent to the phase advance observed on the actogram (Figure 6(A)). However, thefirst and second pulses placed during the hours of the subjective day have caused aslightly reduction of only 20min of the period. Indeed, T. saltator has a nocturnal

0

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80

100

DD

Patte

rns

perc

enta

ge

a c b d e f g pulse n°7pulse n°1 pulse n°2 pulse n°3 pulse n°4 pulse n°5 pulse n°6

unimodal pattern bimodal pattern and plurimodal pattern

Figure 2. Distribution of the different patterns models under the PRC experiment. unimodalpattern; bimodal pattern and multimodal pattern.

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Table

1.Circadian

andUltradianperiod

s(τ24;τ

12)andSNRof

thelocomotor

rhythm

ofT.

salta

torfrom

Bizerte

beach.

DD

Pulse

aPulse

bPulse

cPulse

dPulse

ePulse

fPulse

g

τ 24±SD

24h3

0′±1h2

0′25

h06′±1h2

8′24

h48′±1h0

9′24

h42′±1h0

8′24

h36′±1h5

5′25

h18′±2h0

4′25

h48′±2h5

8′26

h06′±2h3

1′SNR24±SD

.211

±.146

.357

±.253

.418

±.262

.346

±.239

.319

±.284

.245

±.257

.233

±.229

.162

±.191

τ 12±SD

13h1

2′±1h0

0′12

h48′±1h1

4′12

h30′±0h5

1′12

h24′±1h11′

12h2

4′±1h1

2′12

h30′±1h2

0′12

h30′±0h4

9′12

h30′±1h2

8′SNR12±SD

.072

±.076

.130

±.109

.132

±.108

.128

±.155

.130

±.159

.136

±.117

.104

±.076

.080

±.125

Note:

SD=StandardDeviatio

n.

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behaviour and this little training effect can be explained by the application of the pulsesat the neutral zone corresponding to the subjective day (Figure 6(A) and (B)). Afterapplying the fourth pulse, at the beginning of the subjective night, the activity shifted

DD Pulse 1 Pulse 2 Pulse 3 Pulse 4 Pulse 5 Pulse 6 Pulse 7

-0,1

0,1

0,3

0,5

0,7

0,9

20h00

28h00

24h30

Circadian period

SNR

a b c d e f g

Figure 3. Means of periods and SNR measured by periodogram analysis during the PRCexperiment. Vertical bars on each point represent standard deviation (SD).

0,00

0,50

1,00

1,50

2,00

24,4 24,6 24,8 25,0 25,2 25,4 25,6 25,8 26,0 26,2 26,4

Circadian period (hours)

α /ρ

Figure 4. Dependence of activity time (α)/rest time (ρ) ratio over the circadian period.

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to the right. Day after day, the activity started later than expected; it was a phase delayand the period was extended by 60min (Figure 6(A) and (B)). The application of thefifth pulse has resulted a phase advancing with reduction of period τ24 = 23 h: the activ-ity begins rather than planned. Finally, after the application of the two last pulses (sixth

Circadian time (hours)

0

12h 15h 18h 21h 00h 03h 06h 09h 12h

-2

-4

4

2

Phas

e sh

ift (h

ours

)

Figure 5. Superimposed PRCs in T. saltator population.

10H30

12-15

15-18

21-00

03-06

00-03

06-09

18-21

Hours

a

b

c

d

e

f

g

a

b

c

d

e

f

g

1

5

10

15

20

25

30

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60

(A)

Days of experimentj41 j12j7 j65j94j53 j24j82 j63 0

23h 40

23h 20

23h

24h

24h 20

24h 40

25h DD

Pulse a

Pulse b

Pulse c

Pulse d

Pulse e

Pulse f

Pulse g

Cir

cadi

an p

erio

d

(B)

Figure 6. Demonstration of the phase relationship between the synchroniser and the endogenouscomponent of the locomotor rhythm in T. saltator. (A) Double-plotted actogram; (B) PRCcorresponding to this actogram.

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and seventh), again the activity shifted to the right; this result can be explained by thephase delay and the continuous extension of the recorded period (Figure 6(A) and (B)).

Discussion and conclusion

Tunisian T. saltator, like same species and other talitridis from the Mediterranean(Scapini et al. 1992; Mezzetti et al. 1994; Nasri-Ammar & Morgan 2006) and Atlantic(Bregazzi & Naylor 1972; Williams 1983) coasts, show an endogenous nocturnallocomotor activity rhythm (Ayari & Nasri-Ammar 2011). By maintaining specimens ofT. saltator displaying a free-running rhythm during the first week of experience, resultsrevealed that this amphipod exhibits a circadian rhythm with a semi-diurnal componentof about 12 h. According to the literature, this may be caused by the tides’ rhythm(Scapini 1997; Fallaci et al. 1999): landward migration at the time of high water wasinstead expected. Moreover, it can be a strategy to avoid desiccation stress. The train-ing of endogenous rhythmicity by light pulses confirmed the persistence of both circa-dian and ultradian components. In fact, the photic stimuli are the strongest Zeitgebersentraining the molecular clockwork with the external world (Williams 1980). Thephase relationship established is such that the phase of the rhythm entrained by lightstimulus inducing a phase shift equal to the difference between τ and T (Williams1980). Pittendrigh and Daan (1976a) suggest that a major factor contribution to pertur-bations of the stable-phase relationship between biological rhythm and environment,indicative of entrainment, is the systematic seasonal change of photoperiod. Thus,these two authors proposed a non-parametric mechanism of steady-state entrainment,in which the PRC is considered to be the reflection of two mutually interactive oscilla-tors coupled separately to sunset and sunrise and thus, independently controlling the“evening” and “morning” components of the active phase (Pittendrigh & Daan 1976c).Entrainment therefore depends on the interaction of the phase shift exerted by eachoscillator, which would not only be related to τ, but would also be a response of thesystematic variation in the interval of the “evening” and “morning” pulse stimulus, theseasonal change in daily photoperiod (Pittendrigh & Daan 1976b).

Moreover, the PRCs have all obtained a sinusoidal highlighting advance and delayphases to fix the limits of entraining. The entrainment is based on a periodicallychanging sensitivity of the animal to light which is expressed as a PRC (Pittendrigh1960; Aschoff 1965). Furthermore, according to our results, T. saltator was more sen-sitive to the pulses administrated at the subjective night more than those applying atthe subjective day; In fact, the stability of the rhythm was more important and the per-iod was more close to 24 h. Thus, this sensibility can be explained by the nocturnalbehaviour of this species. Williams (1980) showed that the PRCs define, graphically,the phase-dependent variation of the quality and quantity of the sensitivity of theendogenous rhythm during the entire circadian period. The range of entrainment ofthis circadian period varies between 21 h and 29 h 20′. Honma et al. (1985) showedthat in albino rats, an interval of training period ranges between 23 h and 27.3 h as theupper limit.

AcknowledgementThe study was supported by the Research Unit of Animal Eco-Biology and EvolutionarySystematics (UR11ES11), Faculty of Science of Tunis, University of Tunis El Manar.

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19 1

9 N

ovem

ber

2014