JOURNAL OF CRUSTACEAN BIOLOGY, 24(2): 282–290, 2004
LOCOMOTOR ACTIVITY RHYTHMS OF CONTINENTAL SLOPE
NEPHROPS NORVEGICUS (DECAPODA: NEPHROPIDAE)
Jacopo Aguzzi, Joan B. Company, and Pere Abelló
(JA, JBC, PA) Institut de Ciències del Mar – CMIMA (CSIC), Passeig Marı́tim 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 (Sardà, 1995; Abelló 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; Aréchiga 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; Aréchiga 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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AGUZZI ET AL.: DEEP-WATER NEPHROPS LOCOMOTOR RHYTHMS
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 (Abelló 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; Fernández de Miguel
and Aréchiga, 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
283
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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JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 24, NO. 2, 2004
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
AGUZZI ET AL.: DEEP-WATER NEPHROPS LOCOMOTOR RHYTHMS
285
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; Aréchiga 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; Aréchiga 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; Aréchiga 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
AGUZZI ET AL.: DEEP-WATER NEPHROPS LOCOMOTOR RHYTHMS
287
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 (Aréchiga 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., Dı́ez-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
AGUZZI ET AL.: DEEP-WATER NEPHROPS LOCOMOTOR RHYTHMS
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) (Abelló 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;
Aréchiga et al., 1980).
ACKNOWLEDGEMENTS
Special thanks are due to Dr. F. Sardà, Chief Scientist of the
NERIT Project (MAR98-0935) for his support and valuable
comments, and to Prof. E. Naylor, Dr. A. Dı́ez-Noguera,
and Dr. T. Cambras for important suggestions during the
preparation of this manuscript. J. A. Garcı́a 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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RECEIVED: 15 September 2003.
ACCEPTED: 7 January 2004.