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Seasonal variation of locomotor activityrhythm of Orchestia montagui in thesupralittoral zone of Bizerte lagoon(North of Tunisia)Raja Jelassi a & Karima Nasri-Ammar aa Faculty of Science of Tunis , Research Unit of Animal Biology andEvolutionary Systematics, University of Tunis El Manar II , 2092 ,Tunis , TunisiaAccepted author version posted online: 18 Oct 2012.Publishedonline: 16 Nov 2012.

To cite this article: Raja Jelassi & Karima Nasri-Ammar (2013) Seasonal variation of locomotoractivity rhythm of Orchestia montagui in the supralittoral zone of Bizerte lagoon (North of Tunisia),Biological Rhythm Research, 44:5, 718-729, DOI: 10.1080/09291016.2012.739929

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Seasonal variation of locomotor activity rhythm of Orchestia montaguiin the supralittoral zone of Bizerte lagoon (North of Tunisia)

Raja Jelassi* and Karima Nasri-Ammar

Faculty of Science of Tunis, Research Unit of Animal Biology and Evolutionary Systematics,University of Tunis El Manar II, 2092 Tunis, Tunisia

(Received 10 August 2012; final version received 9 October 2012)

Locomotor activity rhythms of Orchestia montagui were investigated in a popula-tion from the supralittoral zone of Bizerte lagoon. These rhythms were recorded inindividual animals over the four seasons under two simultaneous experimentalregimens; during the first week, the animals were kept in light–dark cycle in phasewith the natural diel cycle. During the second week, animals were maintained inconstant darkness (DD). Results revealed that, whatever the season, actograms andmean activity curves showed globally that individuals of O. montagui concentratedtheir activity during the experimental and subjective day. In addition, animalsexhibited a diurnal circadian rhythm of locomotor activity with an ultradiancomponent. Under light–dark cycle, circadian periods determined by periodogramanalysis in four seasons were appreciably similar andwere close to 24 h.While underconstant darkness, circadian period was longer in winter (tDD ¼ 25 h 540 + 1 h 140)and summer (tDD ¼ 25 h 470 + 0 h 450) than in spring (tDD ¼ 24 h 260 + 1 h 510)and autumn (tDD ¼ 24 h 440 + 2 h 220). In addition, the study of the mean activitytimes calculated for four seasons showed that, whatever the regimen imposed, themost important activity of individuals was observed in summer and it was equal to11 h 510 + 5 h 100 and 16 h 270 + 5 h 440 under entraining conditions and constantdarkness, respectively. With reference to environmental stability and variability, thedifferences of locomotor activity characteristics observed are explained as a need forplasticity to adapt to environmental changes.

Keywords: lagoon; locomotor rhythm; entraining conditions; free-running;Orchestia montagui; seasonal variation

Introduction

The biological rhythms are observed in the great majority of alive beings in theexpression of molecular, biochemical, physiological, or behavioral phenomena. Theoccurrence of these phenomena is considered as an adaptation to cyclic variations ofphysical environment. Endogenous circadian rhythm facilitates the adaptation ofanimals to their environment. This rhythm is observed among the most animalsplaced in constant artificial conditions (Aschoff 1960, 1966, De Coursey 1960). Innatural environment, the exogenous components adjust the circadian activityrhythm of animals with daily periodicity of 24 h. The day–night alternation was themost important synchronizer (Aschoff 1986).

*Corresponding author. Email: djelassi.raja@gmail.com

� 2012 Taylor & Francis

http://dx.doi.org/10.1080/09291016.2012.739929Vol. 44, No. 5, 718–729,

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The littoral environment is inhabited by many forms of arthropods; eachcharacterized by particular ecophysiological requirements. Many studies concern thepresence and function of locomotor activities with various types of periodicity (daily,circadian, tidal, lunar, circalunidian, etc.), which anticipate stressful environmentalchanges (Naylor 1985, 1988; Palmer 1995). Many others deal with the identificationof orientation factors and the mechanisms used during homing or zonal recovery(Rebach 1981; Herrnkind 1983; Chelazzi 1992; Wehner 1992).

It has been known for a long time that supralittoral amphipods are mainlynocturnal animals (Verwey 1929; Williamson 1954; Palluault 1954), such as shownby Orchestia gammarellus, Orchestia mediterranea, and Orchestia cavimana (Wildish1970), Talorchestia deshayesii (Williams 1982, 1983; Ayari and Nasri-Ammar 2011a),and Talitrus saltator (Nasri-Ammar and Morgan 2005a, 2006). Whereas, the tidalestuarine species Corophium volutator shows almost exclusively a semidiurnal tidalpattern (Holmstrom and Morgan 1983), which in the sand beach amphipodBathyporeia pelagica is modulated over a circadian period (Fincham 1970a, 1970b).

Similar diurnal modulation of the circatidal pattern of swimming has beenrecorded in the surf-migrant isopod Eurydice pulchra from the European sandbeaches of the North Atlantic, and a circa-semilunar monthly pattern of total dailyswimming is also evident (Reid and Naylor 1985). Studying the locomotor rhythm oftwo sympatric species of talitrids in spring, Jelassi et al. (2012) showed the presenceof two locomotor behaviors diurnal for Orchestia montagui and nocturnal for O.gammarellus. The diurnal behavior characterizes many species of Isopods such asTylos granulatus (Kensley 1974).

Williams (1980) showed that, in constant conditions, the free running activityrhythm of T. saltator remains stable for many days and that the photoperiod,particularly dawn, is the main factor of locomotor activity synchronization. Morerecently, Yannicelli et al. (2000) studied the activity rhythm of two Uruguayancirolanid isopods, which occupy different beach levels, using the field observationsand laboratory experiments. Excirolana armata was seen to be active most of thetime, but laboratory results showed that emergence under constant conditions wasrare. However, individuals of Excirolana braziliensis were always observed duringthe night, and they displayed an endogenous circadian activity.

The present study was aimed to characterize and to estimate the impact of seasonalvariation on the locomotor activity rhythm of O. montagui. Moreover, the seasonalstudy was conducted in order to confirm previous study on the locomotor rhythm ofthis species living in the supralittoral zone of Bizerte lagoon (Jelassi et al. 2012).

Material and methods

Collection site and experimental protocol

Samples of freshly adult of O. montagui from the supralittoral zone of Bizerte lagoonat Menzel Jmil (N37813080E098550100) were collected by hand in the morning duringwinter, spring, summer, and autumn, under Cymodocea banquette, Suaeda maritimaand between Salicornia arabica roots, and they were transported as soon as possibleto the laboratory. For each experience, 30 specimens were individually transferred toseparate annular actographs containing approximately 2–3 cm of sand. Then, theywere kept in a controlled environment cabinet maintained at a constant temperatureof 188C + 18C. Locomotor activity in each actograph was provided with infraredbeam focused across the platform. Interruptions due to animal activity were

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recorded by a data-logger, using the Sand 16 software program and downloaded ona computer every 20 min. The recording apparatus and controlled environmentcabinet were designed and constructed in the School of Biosciences University ofBirmingham, Birmingham, UK.

To characterize the seasonal variation of the locomotor activity rhythm ofO. montagui, four experiences were conducted under two photoperiodic regimens inwinter (sunrise: 7 h 340; sunset: 17 h 130), in spring (sunrise: 5 h 380; sunset: 19 h 010),in summer (sunrise: 4 h 590; sunset: 19 h 380), and in autumn (sunrise: 6 h 570; sunset:17 h 130). The experimental conditions were similar to those described by Nardi et al.(2003) and Scapini et al. (2005). During the first 7 days, animals were kept in light–dark cycle (nLD) in phase with the natural diel cycle; for the rest of experiment (7days), animals were maintained under constant darkness (DD).

Data analysis

The results were initially presented for analysis in the form of actograms showingactivity accumulated over 20 min, using the Chart software package version 35 (D.D.Green, University of Birmingham, UK). This provided the option of normalizing thedata by expressing each datum point as a percentage of the highest value for the 24 hover which it occurred or the highest value over the entire time series (Cummings andMorgan 2001). Subsequent periodogram analysis was performed using the programbased on the method of Dorscheidt and Beck (Harris and Morgan 1983). Each timeseries was scanned for periods between 10 h and 33 h 200 and was accepted asrhythmic if the periodogram peaks exceeded the 99% confidence level.

The percentage of mortality, number of animals showing periodicity, meancircadian period, and the signal noise to ratio (SNR) were calculated for eachindividual from the collected data. The definition of the period (SNR) was calculatedas the ratio between the correlation ratio of the periodogram and the 95% pro-bability line in the periodogram analysis and was used as a measure of the definitionof the rhythm. All the periods mentioned here were significant at the p 5 0.05 level.Non-significance, where mentioned, corresponded to p 4 0.05.

The waveform of activity was further examined using the astronomic time underentraining conditions and circadian time under free-running conditions. Phase valueswere calculated using a technique in which the median point of the main activity blocis correlated to the time of onset of the dark phase, expressed in degrees. Activitytime (a) can clearly be separated from rest time (r) by considering the initiation andcessation of significant activity.

Statistics analyses were based on non-parametric tests. The differences betweenall mean values were estimated using the Wilcoxon (comparison between twosamples) and Kruskal–Wallis rank tests (comparison between three or moresamples), whereas, the differences between percentages were calculated using the w2

tests.

Results

Mortality and rhythmicity

Our data showed that, in the end of these experiences, among 120 specimens, only 52survived for 15 days in the recording chambers. Mortality was significantly higher inspring (80%) and autumn (87%). Under nLD cycle, actograms analysis showed a

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concentrated activity during the experimental day in winter, spring and summer. Inautumn, this activity was concentrated during the experimental night (days: 1, 2, 6,and 7) and day (days: 3, 4, and 5) (Figure 1). Under constant darkness, a clear driftwas observed only in winter and summer. This activity was spread over the day inspring and autumn (Figure 1).

We observed that not all animals were rhythmic. Moreover, both ultradian andcircadian rhythmicities components were determined whatever the season except inwinter and summer, when animals were maintained under constant darkness, onlycircadian rhythmicity was observed. In fact, under entraining conditions (nLD),ultradian rhythmicity was statistically more important in spring (50%) and summer(63.3%) than in winter (23.3%) and autumn (20%) (w2 ¼ 16.61, df ¼ 3, p ¼ 0.0008).Under constant darkness, ultradian rhythmicity was determined only in spring andautumn with the same percentage (16.7%). Concerning the circadian rhythmicity, itwas significantly greater during summer both under light–dark cycle (w2 ¼ 11.96,df ¼ 3, p ¼ 0.0075) and constant darkness (w2 ¼ 12.54, df ¼ 3, p ¼ 0.0057). Duringthis season, the percentage of circadian rhythmicity was equal to 86.7% and 60%,respectively (Table 1).

Locomotor activity pattern

Under entraining conditions, locomotor activity patterns are in majority unimodal;their percentage were equal to 76.5% in winter, 56.5% in spring, 100% in summer,and 58.8% in autumn. Under free-running conditions, the multimodal profilecharacterize the fall and spring seasons with 100% and 80%, respectively. On theother hand, the most important activity peak was closed to the transition dark/lightin winter (76.9%), spring (87%), and summer (100%) under entraining conditions.In autumn, whatever the regimen, this peak was closed to the transition light/dark(Figure 2).

Parameters of locomotor activity rhythm

Through periodogram analysis, both circadian and ultradian period are obtainedunder entraining condition. These periods are close to 24 h and 12 h, respectively,and are approximately equal between seasons (Figure 3, Table 1). Under free-running conditions, only in spring and autumn, we observed ultradian period;it was equal to tDD12h ¼ 12 h 360+ 2 h 060 and 11 h 440+ 0 h 580, respectively.For circadian period, it changed between seasons; it was longer in winter(tDD24h ¼ 25 h 540+ 1h 140) and summer (tDD24h ¼ 25 h 470+ 0 h 450) than inspring (tDD24h ¼ 24 h 260+ 1 h 510) and autumn (tDD24h ¼ 24 h 440+ 2 h 220)(Table 1). Extending of circadian period in winter and summer was related to theclear drift observed in actograms (Figure 3, Table 1).

To obtain more objective estimates for seasonal comparison, SNR valuesderived from the periodograms of individual animals have therefore been used. TheSNR was estimated both for circadian and ultradian components. Rhythm wasstatistically more stable and better defined in summer than in the other seasonsunder entraining conditions (w2 ¼ 27.291, df ¼ 3, p ¼ 0) and constant darkness(w2 ¼ 16.058, df ¼ 3, p ¼ 0.0011) (Table 1).

Finally, study of activity times calculated in different seasons showed that, underentraining conditions, the most important activity of animals was recorded in

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summer (aLD24h ¼ 11 h 510+ 5 h 100). Kruskall–Wallis rank test showed a highersignificant difference in activity times between seasons under free-running conditions(w2 ¼ 14.48, df ¼ 3, p ¼ 0.0023) (Table 1). In fact, intensity of activity became moreimportant in summer (aDD24h ¼ 16 h 270+ 5 h 440) under constant darkness.Moreover, there is an important dispersion of activity time showing a high individualvariability (Table 1).

Figure 1. Double plotted actograms of the locomotor activity rhythm of Orchestia montaguiunder LD-DD observed in winter (A), spring (B), summer (C), and autumn (D). Grey areacorresponds to dark; #Light-dark transition; "Dark-light transition.

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Figure

2.

Waveform

soflocomotoractivityrhythm

ofOrchestiamontaguiunder

LD-D

Din

differentseasons.

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Figure

3.

Periodogramsoflocomotoractivityrhythm

ofOrchestiamontaguiunder

LD-D

Din

differentseasons.

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Table

1.

Summary

statisticsofactivityrhythmsparametersrecordingsunder

LD-D

D.

Winter

Spring

Summer

Autumn

w2test

Kruskal–Wallis

ranktest

LD

Mortality

20

80

40

87

HS(p¼

0)

Rhythmicity12h(%

)23.3

50

63.3

20

HS(p¼

0.0008)

Rhythmicity24h(%

)56.7

76.7

86.7

50

HS(p¼

0.0075)

Pdg12+

SD

12h140 +

1h010 N

S11h550 +

0h520

12h020 +

0h090

12h+

0h550

NS(p¼

0.397)

Pdg24+

SD

24h070 +

1h030

24h220 +

0h540

24h140 +

0h460

24h290 +

1h310

NS(p¼

0.572)

Snr12+

SD

0.127+

0.063

0.144+

0.116

0.428+

0.225

0.180+

0.035

HS(0.0003)

Snr24+

SD

0.225+

0.121

0.195+

0.109

0.603+

0.328

0.184+

0.09

HS(p¼

0)

Activitytime(a)+

SD

9h350 +

5h000

9h500 +

4h160

11h510 +

5h100

8h380 +

6h300

NS(p¼

0.218)

Resttime(r)+

SD

14h320 +

5h000

14h320 +

4h430

12h230 +

5h230

15h510 +

6h240

NS(p¼

0.165)

DD

Rhythmicity12h(%

)–

16.7

–16.7

Rhythmicity24h(%

)43.3

33.3

60

16.7

HS(p¼

0.0057)

Pdg12+

SD

–12h360 +

2h060

–11h440 +

0h580

NS(p¼

0.671)

Pdg24+

SD

25h540 +

1h140

24h260 +

1h510

25h470 +

0h450

24h440 +

2h220

NS(p¼

0.124)

Snr12+

SD

–0.117+

0.077

–0.128+

0.035

NS(p¼

0.420)

Snr24+

SD

0.243+

0.208

0.105+

0.108

0.416+

0.338

0.075+

0.028

HS(p¼

0.0011)

Activitytime(a)+

SD

9h010 +

4h430

9h030 +

6h230

16h270 +

5h440

4h220 +

6h030

HS(p¼

0.0023)

Resttime(r)+

SD

16h530 +

4h530

15h230 +

6h140

9h180 +

6h00

20h220 +

07h470

HS(p¼

0.0032)

Note:LD,light–dark;DD,constantdarkness;

SNR,signalnoiseto

ratio;SD,standard

deviation;12and

24indices

correspond

toultradian

and

circadian

period,

respectively;S,significant;HS,highsignificant;NS,nosignificant.

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Phase delay and phase advance of the endogenous rhythm of O. montagui

Phase shift analysis, technically possible not for all individuals, varied betweenseasons. In summer, autumn, and winter, it is a phase delay with a mean phaseshift equal to 711.68 + 728, 714.58 + 928, and 723.48 + 1078, respectively. Thisresult explains the activity drift observed on the actograms under DD conditionsespecially in winter and summer and more or less in autumn. In fact, this phase shiftmakes periods longer from day to day. Whereas, in spring, it is a phase advanceequal to 3.78 + 318. Moreover, Kruskall–Wallis rank test revealed no significantdifference between seasons.

Discussion

The locomotor activity pattern recorded for O. montagui in the present study wastypical to other animal species such as T. granulatus (Kensley 1974), Hemilepistusreaumurii (Nasri-Ammar and Morgan 2005b), Melanoides tuberculata (Beestonand Morgan 1979), Culex pipiens (Chiba 1964), and Anopheles gambiae (Joneset al. 1972), which displayed diurnal behavior. Their activity was concentratedduring the experimental and subjective day in winter and summer and more orless in the other seasons where we observed a mixed behavior, diurnal andnocturnal. The mixed behavior observed in spring and autumn may be explainedby the seasonal migration during these seasons from coastline to dune system inautumn and from dune system to coastline in spring. Moreover, these twoseasons are characterized by the high mortality; this result may be correlated withthe life cycle of animal and longevity.

Contrary to O. montagui, many other amphipods and terrestrial isopods wereactive during the night, such as O. gammarellus (Jelassi et al. 2012), T. saltator (Bohliet al. 2006; Nasri-Ammar and Morgan 2005a, 2006), Talorchestia deshayesii(Williams 1982, 1983; Ayari and Nasri-Ammar 2011a), Tylos europaeus (Bohli-Abderrazak et al. 2012), O. mediterranea, and O. cavimana (Wildish 1970).

Under free-running conditions, a remarkable drift of the activity rhythmespecially in summer and winter was observed explaining the extension of thecircadian period. Waveform curves showed that, under entraining conditions, themajority of locomotor patterns were unimodal whatever the seasons, and specimenswere more sensitive to the experimental dawn expect in the autumn. Under constantdarkness, the plurimodal profile characterized spring and autumn, and animals weremore sensitive to the experimental dusk. This multiplication of activity peak maycorrespond to their various activities in the field, such as burrowing activity orforaging activity or the prospecting of new habitats (Ayari and Nasri-Ammar2011a).

Otherwise, our results showed that circadian rhythmicity varied from season toseason as demonstrated by Nardi et al. (2003) by examining an Italian populationof T. saltator. Whatever the regimen imposed, the most important circadianrhythmicity was observed in summer. The same result was found by Nardi et al.(2003). Whereas, the lowest rhythmicity was observed in autumn; studying the twoTunisian populations of T. saltator in Korba and Barkoukech (North easternTunisia), Nasri-Ammar and Morgan (2005a, 2006) showed that the lowest circadianrhythmicity was observed in summer and autumn, respectively.

Periodogram analysis showed that animals of O. montagui exhibited circadiancomponent of about 24 h whatever the seasons. This period lengthened under

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constant darkness. This result confirms that the light–dark cycle was a powerfulsynchronizer of O. montagui locomotor activity rhythm as has been demonstrated byBregazzi and Naylor (1972), Williams (1980), Nasri-Ammar and Morgan (2006a),Ayari and Nasri-Ammar (2011a, 2011b). Bohli-Abderrazak et al. (2012) reportedalso that the locomotor activity rhythm of T. europaeus was predominantlysynchronized by the experimental LD cycle.

Under constant darkness, the shorter period of O. montagui specimens wasrecorded in spring and autumn. The study of seasonal variation of T. saltator fromBarkoukech beach showed shorter free-running periods during coldest season(Nasri-Ammar and Morgan 2006). On the other hand, Nardi et al. (2003), studyingItalian population of T. saltator from Castiglione della Pescaia, found shorter free-running periods during the summer months; these authors attributed this result tothe need to synchronise the activity more closely to the solar day and to escape thehigh temperature and the low humidity prevailing at this time. This seasonalvariation of circadian period is probably to be a function of the endogenoustimekeeping system and not to seasonal environmental changes (Ayari and Nasri-Ammar 2011a)

In addition, an ultradian component close to 12 h was observed. The existence ofthe ultradian rhythm suggested a sensibility of the animal to tidal movements despitetheir very low amplitude in the study site. This ultradian component may be causedby the tide’s rhythm (Scapini 1997; Fallaci et al. 1999): landward migration at time ofhigh water was instead expected. Moreover, it can be a strategy to ovoid desiccationstress. This component was found for O. gammarellus population in the supralittoralzone of Bizerte lagoon (Jelassi et al. 2012). Wildish (1970), in a comparative study,recorded circatidal rhythms in a semi-terrestrial amphipod living below the high-water mark under stones; whereas, no clear tidal component was evident inO. cavimana, a freshwater and estuarine species, and in O. gammarellus that colonizethe littoral above the recent high-water mark. Moreover, a tidal periodicity wasobserved in phase with the semidiurnal and monthly tides in the two sympatricspecies Talorchestia brito and T. saltator (Fallaci et al. 1999). The circatidal rhythmwas also observed for Tunisian population of T. europaeus (Bohli-Abderrazak et al.2012).

Furthermore, under entraining conditions, the most important stability oflocomotor activity rhythm was observed in summer both for semi-diurnal andcircadian components. This highest circadian stability persisted under constantdarkness in summer. Rossano et al. (2008) showed also that activity rhythms ofO. montagui and T. saltator were similar, with a good definition and precise circadianperiodicity, whereas O. gammarellus showed a high variability and low definition ofthe circadian rhythm. Ayari and Nasri-Ammar (2011a) showed that the higherstability of T. saltator activity rhythm was revealed in spring.

This present study highlighted the presence of diurnal behavior in O. montaguithat living in sympatric with other nocturnal species and shared the same food.Then, the absence of overlap between temporal niches has suggested as anadaptative strategy in order to minimize interspecific competition (Jelassi et al.2012).

Acknowledgement

The study was supported by the Research Unit of Bio-ecology and Evolutionary Systematics(UR11ES11), Faculty of Science of Tunis, University of Tunis El Manar.

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