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LOCOMOTOR ACTIVITY RHYTHMS OF CONTINENTAL SLOPE NEPHROPS NORVEGICUS (DECAPODA: NEPHROPIDAE) Jacopo Aguzzi, Joan B. Company, and Pere Abello´ (JA, JBC, PA) Institut de Cie`ncies del Mar – CMIMA (CSIC), Passeig Marı´tim de la Barceloneta 37-49, 08003 Barcelona, Spain (JA, corresponding author:
[email protected], Neurophysiology Institute, Morehouse School of Medicine, 720 Westview Drive, S.W., Atlanta, Georgia, 30310, U.S.A.) ABSTRACT The locomotor rhythmicity of the Norway lobster Nephrops norvegicus was studied under constant conditions of darkness in individuals collected on the continental slope (400–430 m). Periodogram analysis revealed the occurrence of both circadian (of around 24 h) and ultradian (of around 12 and 18 h) periodicities. Form estimate analysis of the circadian and ultradian time series revealed the occurrence of significant peaks of activity during the expected night phase of the cycle and day-night transitions, respectively. No ultradian locomotor activity rhythms have been reported in previous studies on continental shelf N. norvegicus, suggesting that this phenomenon may be limited to deep-water animals. A discussion is presented to account for the occurrence of the mechanism of ultradian rhythms when there is significant environmental light intensity reduction, as on the continental slope, where the species attains its maximum densities in the western Mediterranean.
One aspect of animal behaviour consists of movement patterns linked to physical or biological environmental variables, which may be of a cyclic nature. Rhythmic behaviour, in particular, encompasses all motor acts that involve a rhythmic repetition coupled to a cyclical variable (Naylor, 1988; Nusbaum and Beenhakker, 2002). Among rhythmic behavioural processes, locomotion is the most widely studied indicator in biological clock regulation research (Naylor, 1988; Ortega-Escobar, 2002). Nephrops norvegicus (L.) is a burrowing decapod that inhabits the muddy continental shelf in the Northeast Atlantic (Farmer, 1975). Its distribution extends into much deeper areas on the continental slope in the Mediterranean Sea (Sarda`, 1995; Abello´ et al., 2002a, b). Marked depth-dependent rhythms of emergence from burrows are present in this species. Its timing changes from nocturnal on the shallow continental shelf to crepuscular with peaks at sunset and sunrise on the deep continental shelf, and diurnal on the continental slope (Farmer, 1974; Chapman and Howard, 1979; Oakley 1979; Moller and Naylor, 1980; Aguzzi et al., 2003). Optimum light intensity has been considered the main environmental cue for these rhythms (Chapman et al., 1975). Nephrops norvegicus from the continental shelf, from the subtidal down to 180 m depth, has been shown to exhibit a marked endogenous
locomotor rhythmicity under constant darkness conditions (Atkinson and Naylor, 1976; Are´chiga et al., 1980) whose periodicity and phase are depth-independent. The comparison of laboratory data on locomotor activity rhythms with field catch patterns to account for emergence behaviour in the population revealed a phase discrepancy with increasing depth. Thus, the rhythmic patterns of endogenous locomotion showed the same characteristics of circadian periodicity with nocturnal phase in animals from the shallow subtidal to the lower shelf (Atkinson and Naylor, 1976; Are´chiga et al., 1980), whereas trawl catch patterns accounting for emergence from burrows varied from a nocturnal pattern on the upper shelf to a crepuscular one with peaks at sunset/ sunrise hours on the lower shelf (Atkinson and Naylor, 1976; Chapman and Howard, 1979). Light intensity was hypothesised to be the main environmental cue for the bathymetric dissociation of emergence from endogenous locomotion. Previous published behavioural studies of N. norvegicus have been restricted to the continental shelf populations in the NE Atlantic, and deep-water data are lacking. In deep areas, light intensity is much reduced, although still capable of prompting a full daytime emergence (Aguzzi et al., 2003). Therefore, the present research was planned to determine the pattern of endogenous locomotor rhythmicity, if any, expressed by deep-water N. norvegicus inhabiting
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the continental slope. Studies of this kind are important to understand how endogenous locomotion is expressed in an environmental context of significant light intensity reduction. MATERIALS AND METHODS The locomotor activity patterns of N. norvegicus were studied under laboratory conditions of constant darkness and temperature. A total of 28 adult males with carapace lengths (CL) between 31 and 40 mm was monitored. These individuals were freshly collected from around 400–430 m depth by a commercial trawler that operated in the western Mediterranean Sea a few miles off Barcelona (41819N, 18379E; 408559N, 18319E). Difficulties in catching live individuals and bringing them back to the laboratory in good physiological condition precluded the testing of a much larger number of individuals. The experimental temperature of 13 6 0.18C was set to match the environmental temperature of the western Mediterranean continental slope found throughout the year (Salat, 1996). To avoid biases in data records because of interference of the moulting metabolism and sexual stage on behavioural performance, only adult males in the intermoult stage were monitored. The selected individuals were immediately transferred on board to aerated containers and taken to the laboratory within two hours. An infrared-sensitive video camera connected to a timelapse video recorder was used with a constant source of infrared light to record the number of times that an individual crossed a vertical reference line in 30 min intervals. The experimental set-up was performed similarly to previous studies on decapod crustacean behavioural rhythms (Abello´ et al., 1991; Guerao, 1995; Guerao and Ribera, 1996; Borst and Barlow, 2002; Forward et al., 2003). During the tests, each animal was individually housed in a plastic tank (40 3 25 3 20 cm) supplied with an external pump providing the appropriate circulation and filtration of water. Isolation was necessary to avoid possible biases in the recorded rhythmicity because of synchronising effects through dissolved metabolites. The animals were not fed during the experiments to prevent interference because of food presence-absence, which directly affects locomotor activity and metabolism (Ansell, 1973; Ferna´ndez de Miguel and Are´chiga, 1994). To reduce handling stress to a minimum prior to the start of the experiment, all individuals were sized at the end of each test. The temporal series of raw data were smoothed with a three-point moving average to eliminate high-frequency noise ( 1.5 h) (Levine et al., 2002). Periodogram analysis was performed to determine inherent periodicities in the recorded time series of data and was used to screen the time series for periodicities between 4 h and 30 h (Aagaard et al., 1995). Thus, a wide array of rhythms including circadian and ultradian could be identified. In the resulting plot, peaks indicating the inherent significant periodicity correspond to those crossing the 95% upper-limit confidence interval. The rhythmic time series of data were transformed into form-estimates to identify the phase of the rhythm. To extrapolate the results obtained on the endogenous locomotor activity to the field context, and therefore to relate them to records on emergence behaviour at a corresponding depth (Aguzzi et al., 2003), all form-estimates were calculated on a 24 h basis (adapted from Kennedy et al., 2000) as follows: all the temporal series of data were set up in rows of 48
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values (one value every 30 min); then, for each time interval, all coinciding values of the subseries were averaged and represented over 24 h along with their standard deviation. Two adjacent peaks were distinguished as significantly different only when separated by three or more values below the 24 h mean (Warman and Naylor, 1995). To determine in which phase of the day-night cycle significant peaks in formestimates were distributed, their frequencies were calculated in 3-h time intervals.
RESULTS Of the 28 animals surveyed, 25 (89.3%) exhibited a significant locomotor rhythmicity, whereas only 3 (10.7%) showed arrhythmia in their locomotor patterns. The smoothed temporal series of movements of two representative individuals are reported as an example in Fig. 1. The locomotor rhythmic patterns presented were clear, although some variability over short time intervals was present as a typical feature of invertebrate behavioural rhythms (e.g., Palmer and Williams, 1986a, b; Dowse and Ringo, 1994). The locomotor activity rhythm of the individual reported in Fig. 1A was characterised by peaks of activity occurring during the expected night phases. The locomotor activity rhythm recorded for the individual shown in Fig. 1B was more complex, and was characterised by a multiple peak profile over the 24 h cycle. Concerning the time series reported in Fig. 1A, periodogram analysis detected a significant circadian periodicity (Fig. 2A), whereas in the data presented in Fig. 1B, a significant periodicity at around 12 h was found (Fig. 2B). The frequency distribution of significant periods detected by periodogram analysis showed the occurrence of three characteristic groups (Fig. 3). The most important one was composed of 14 animals (56.0%) that expressed a circadian locomotor rhythmicity with recorded significant periods of between 20 and 25 h. A second group was composed of 8 animals (32.0%) that showed an ultradian periodicity of around 12 h. Finally, a third, smaller group (3 individuals, 12.0%) was composed of animals expressing ultradian periodicities of around 18 h. As a second step of the analysis, the phase of all circadian and 12-h ultradian rhythms was assessed by computing the corresponding formestimates. The form-estimate analysis of time series presenting ultradian 18 h periodicity was not performed because this periodicity is not a submultiple of the circadian one and cannot be represented on a 24 h basis. Figure 4 shows the form-estimates of the data series presented in Figs. 1A and 1B. In the animal showing
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Fig. 1. Smoothed time series of numbers of movements per 30 min time interval for two individuals of Nephrops norvegicus expressing different locomotor activity patterns, with a single peak (A) and more than a single peak (B) per day. nn, expected night.
a circadian locomotor activity rhythm (Fig. 4A), the peak of activity was phased with the expected night. The animal showing the ultradian 12 h periodicity (Fig. 4B) showed two locomotor activity peaks per 24 h cycle, phased after expected sunset and sunrise. The frequency distribution per 3-h time interval of significant activity peaks recorded in the form estimates of all circadian and 12 h ultradian time series is presented in Fig. 5. Animals expressing a circadian periodicity (Fig. 5A) broadly showed peaks of activity during the
expected night phase and expected hours of day/ night transitions, with a majority of peaks occurring during the first half of the night. Ultradian animals (Fig. 5B) behaved differently, with the two peaks constituting their bimodal profile approximately concentrated during the expected hours of day/night transitions. DISCUSSION The present investigation indicated that deepwater Nephrops norvegicus inhabiting the continental slope showed a marked endogenous
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Fig. 2. Periodogram analysis of the time series presented in Fig. 1, showing significant periodicities with the corresponding 95% confidence interval (dotted lines) (A: circadian periodicity; B: ultradian periodicity).
locomotor rhythmicity. Both circadian periods of around 24 h and ultradian periods of less than 20 h were found. Animals expressing a circadian rhythmicity confirm previously published findings for shallower water conspecifics in the Atlantic (Atkinson and Naylor, 1976; Hammond and Naylor, 1977; Are´chiga et al., 1980), while the occurrence of ultradian rhythms in some individuals added new information on the behavioural repertoire of this species. In fact, no
ultradian rhythms had been reported in similar studies when continental shelf N. norvegicus had been tested (Atkinson and Naylor, 1976; Hammond and Naylor, 1977; Are´chiga et al., 1980), suggesting that ultradian rhythms could be a unique feature of deep-water living N. norvegicus. Most monitored individuals recorded in the present study expressed a circadian pattern of locomotion with significant peaks during the
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Fig. 3. Number of animals showing significant period detected by periodogram analysis on the time-series data.
expected night. None of them showed activity peaks concentrated during the expected daytime. These data fit the already described trend of phase dissociation between endogenous locomotor activity rhythm and emergence from the burrow recorded from the shallow to the deep continental shelf (Atkinson and Naylor, 1976; Chapman and Howard, 1979). The recorded rhythmicity patterns of continental slope animals enlarge this tendency over the entire depth range of the species distribution. Cyclical trawl surveys performed continuously over four days on the western Mediterranean continental slope at around 400 m depth pointed out a fully diurnal emergence rhythm in N. norvegicus (Aguzzi et al., 2003). This pattern of emergence is not sustained by a concomitant rise in endogenous locomotion, as shown by most laboratory-tested animals. In fact, the extrapolation of the present results to the field indicates that the locomotor activity rate of these animals increases inside their burrows. This observation is corroborated by the fact that animals transferred to constant laboratory conditions do not show a locomotor rise during the expected daytime hours, the hours of emergence in the field. However, when animals are transferred to constant darkness and the light stimulus is absent, endogenous nocturnal regulation is immediately revealed, while no marked exogenous locomotion during the expected daytime emergence phase takes place. This suggests that diurnal ‘‘optimum’’ light in-
tensity does not mask endogenous locomotion in animals inhabiting the continental slope. An increase in locomotor activity during the nocturnal phases of burrow occupancy raises questions about the ecological significance of this behaviour. Atkinson and Naylor (1976) and Naylor (1988) stated that the nocturnal increase in locomotor activity recorded in constant laboratory darkness during the expected night phases could be explained in terms of burrow maintenance behaviour. Previous work showed that N. norvegicus are endogenously active at night throughout the continental shelf (Atkinson and Naylor, 1976; Are´chiga et al., 1980), and they are also active at night on the continental slope (present results). The nocturnal increase in endogenous locomotor activity could be considered as an endogenous signal to start the nocturnal emergence in animals inhabiting the continental shelf. The adaptive value of biological rhythms is to predict the onset of favourable environmental conditions (e.g., Naylor, 1988, 1992; Ronnenberg and Merrow, 2002) such as ‘‘optimum’’ light intensity. On the shallow continental shelf, emergence is fully nocturnal (Moller and Naylor, 1980) and sustained by a concomitant increase in underlying endogenous locomotor activity. On the continental slope, however, the diurnal emergence is not sustained by the timing of the endogenous rise in locomotion. This may be the result of a biological clock that may be unable to adjust to
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Fig. 4. Twenty-four h form estimate of a circadian (A) and 12 h ultradian (B) time-series data. nn, expected night; —, diel mean numbers of movements (A: 7.46; B: 3.87).
the timing of an ‘‘optimum’’ light intensity occurring during daytime in deep waters. This observation implies that ‘‘optimum’’ light intensity may act as a zeitgeber only on the continental shelf. On the deeper continental slope, the control exerted by light is therefore increasingly exogenous. The mechanisms generating the ultradian rhythms recorded in this study are not easily
explainable. Studies in Drosophila pointed out that light controls locomotor activity via hormonal control (e.g., Scully and Kay, 2000; Taghert, 2001; Malpel et al., 2002). Other marine invertebrates such as the mollusk Bulla possess ocular circadian pacemakers controlling locomotor behaviour (e.g., Roberts and Xinying, 1996; Page et al., 1997). In decapod crustaceans, a hormonal control of locomotor activity
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Fig. 5. Frequency distribution per 3 h time intervals of significant peaks recorded by form estimate analysis of circadian (A) and 12 h ultradian (B) time series. nn, expected night.
is mediated via NDH secretion by the sinus gland in the eyestalks (Are´chiga and RodriguezSosa, 1997). For some decapod species, light has been shown to trigger the coupling of different circadian oscillators into a functional circadian clock (e.g., Palmer, 1989; Dowse and Palmer, 1990; Reid and Naylor, 1990; 1993; Warman and Naylor, 1995; Palmer, 2000). The idea of a global manifested periodicity as a result of the coordinated functioning of different oscillators depending on environmental light conditions has also been proposed for different
taxa, such as mammals (e.g., Dı´ez-Noguera, 1994; Vilaplana et al., 1995; Herzog and Schwartz, 2002). A combination of environmental dim light intensity and phase opposition between endogenous and exogenous (i.e., emergence) regulation of locomotor behaviour may result in the non-functioning of the mechanism controlling locomotor activity with the consequent generation of ultradian rhythms. Ultradian rhythms could therefore be recorded in a consistent proportion of the population inhabiting continental
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slope grounds. The ‘‘optimum’’ light intensity strictly takes place during daytime at this depth. Additionally, dim light-intensity conditions occurring on the slope may prompt a phase shift in the functioning of different circadian oscillators. Animals showing an ultradian 12 h periodicity in their locomotor activity could not be considered as expressing a behavioural adaptation to tidal influences, given the fully subtidal distribution range of this species in the study area (58– 740 m) (Abello´ et al., 2002b). The estimateforms of their locomotor activity rhythm (see Fig. 4B) are similar to those of the bimodal trawlcatch patterns recorded on the lower continental shelf (Oakley, 1979; Moller and Naylor, 1980; Aguzzi et al., 2003). Peaks in catches on the continental shelf occur at sunset and sunrise because of the emergence pattern of the population (Chapman et al., 1975; Chapman and Howard, 1979; Oakley, 1979; Aguzzi et al., 2003). The form-estimate profile of animals expressing a 12 h locomotor rhythmicity also shows two well-distinguished peaks per day, at sunset and sunrise (Fig. 5). The coupling of these data with field results suggests that an endogenously sustained emergence is still possible on the lower shelf. Emergence from the burrows on the shelf is therefore not fully disconnected from endogenous locomotion, and at least some animals may express two endogenous bursts in locomotion at sunset and sunrise corresponding to the emergence timing of the population. In fact, ‘‘optimum’’ light intensity at day/night transitions prompts an emergence that partially anticipates (at sunset) and delays (at sunrise) the onset of endogenous nocturnal locomotion. This notwithstanding, previous laboratory studies with lower continental shelf animals did not show the occurrence of an endogenous bimodal locomotor pattern (Atkinson and Naylor, 1976; Are´chiga et al., 1980). ACKNOWLEDGEMENTS Special thanks are due to Dr. F. Sarda`, Chief Scientist of the NERIT Project (MAR98-0935) for his support and valuable comments, and to Prof. E. Naylor, Dr. A. Dı´ez-Noguera, and Dr. T. Cambras for important suggestions during the preparation of this manuscript. J. A. Garcı´a provided valuable technical support. The authors wish to thank the master and crew of the fishing vessel ‘‘Maireta III’’ for their sampling assistance. This investigation was funded by the Spanish CICYT.
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