Marine Ecology. ISSN 0173-9565
ORIGINAL ARTICLE
Ontogenetic and gender-modulated behavioural rhythms in the deep-water decapods Liocarcinus depurator (Brachyura: Portunidae), Munida tenuimana and Munida intermedia (Anomura: Galatheidae) Jacopo Aguzzi, Joan Baptista Company & Jose´ Antonio Garcı´a Institut de Cie`ncies del Mar (ICM, CSIC), Passeig Marı´tim de la Barceloneta, Barcelona, Spain
Keywords Brachyaran crab; burying behaviour; circadian rhythms; continental slope; crustaceans; deepsea; galatheid crabs; light intensity; Liocarcinus depurator; Munida intermedia; Munida tenuimana; nocturnal; shelf diurnal. Correspondence J. Aguzzi, Institut de Cie`ncies del Mar (ICM, CSIC), Passeig Marı´tim de la Barceloneta 37-49, 08003 Barcelona, Spain. E-mail:
[email protected] Accepted: 10 May 2008 doi:10.1111/j.1439-0485.2008.00252.x
Abstract The regulation and expression of biological rhythms with respect to sex and ontogeny in deep-water benthic decapod crustaceans constitutes an exciting field in marine biology that is far from understood. Liocarcinus depurator, Munida intermedia and Munida tenuimana are ecologically key crustacean decapod species of the Atlantic and Mediterranean shelves and slopes, and their activity rhythms in the field are poorly known. Our aim was to measure the behavioural rhythms of these species, while at the same time defining their type of displacement (i.e. endobenthic, nektobenthic or benthopelagic). Whether gender and ontogeny modulate the rhythmic behaviour of these decapods is unknown, and we sought to clarify this issue. A temporally scheduled series of trawl hauls and light intensity measures was performed on the western Mediterranean shelf (100–110 m depth) and slope (400–430 m), close to the autumn equinox and the summer solstice. The sex and the size of animals in the catches were analysed. Catch patterns were evaluated through waveform and periodogram analyses. Liocarcinus depurator was captured at night on the shelf, whereas on the slope, animals displayed peaks both in the middle of the day and night. Size-related differences (but no gender differences) were found in its rhythmic behaviour, possibly due to intra-specific competition (e.g. fighting) between juveniles and adults. Munida intermedia were weakly diurnal in October and both diurnal and nocturnal in June. Munida tenuimana presented no discernible rhythmicity in October, but was nocturnal in June. Both species showed no evident sex or size modulation of their behaviour. Data were interpreted assuming that all tested species present an endobenthic behaviour (i.e. animals emerge from the substrate during the active phase of their behavioural cycle).
Problem The expression and modulation of biological rhythms in deep water decapod crustaceans is an exciting field of marine biology that is far from understood (Naylor 2005). Species present behavioural rhythms as a response to different environmental fluctuations (e.g. light intensity, tidal or moon cycles) to maximize fitness (Naylor
1985). In subtidal neritic areas, available data indicate that species mostly regulate their behavioural rhythms according to the day–night cycle in a way that often differs depending on their type of displacement. For example, vertically migrating (i.e. pelagic) species are generally nocturnal, as animals actively swim up into the upper layers of the water column at nighttime to forage under the protection of darkness (Herring & Roe 1988). Conversely,
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
93
Aguzzi, Company & Garcı´a
Behavioural rhythms of deep water crustacean decapods
nektobenthic species perform diurnal displacements along the seabed (Moreno-Amich 1994), actively swimming from deeper water areas of the slope (e.g. Cartes et al. 1993) to forage on descending benthopelagic prey (e.g. Sarda` et al. 2003; Fanelli & Cartes 2004; Aguzzi et al. 2007). Less motile benthic species can be classified as endobenthic when animals hide in the sediment at some point during their behavioural cycle. Endobenthic animals are defined as either burrowers when they dig tunnels, or buriers when they cover their body with the sediment (Bellwood 2002). Finally, epibenthic animals simply reside on the seabed (Moreno-Amich 1994). Ecologically equivalent co-existing species use temporal partitioning (as regulated by circadian rhythms) to reduce their inter-specific competition for similar habitat resources (Kronfeld-Schor & Dayan 2003). Conversely, synchronic behavioural rhythms are reported between predator and prey species (Pittman & McAlpine 2001). Also, behavioural rhythms can be modulated based on the sex or size of animals, limiting their intra-specific competition (e.g. Yamaguchi et al. 2004). In the western Mediterranean, the swimming crab Liocarcinus depurator (Linnaeus, 1758) and the squat lobsters Munida intermedia (A. Milne-Edwards & Bouvier, 1899) and Munida tenuimana (Sars, 1872) are the dominant species of the shelf and slope communities (Abello´ et al. 1988, 2002). Their behavioural rhythms and displacement patterns are poorly known. Given their different swimming and movement abilities (Company & Sarda` 1998), they may regulate their behaviour differently, and this regulation may be different in males, females, juveniles and adults. Liocarcinus depurator has been indicated as a burier (Hall et al. 1990) that is nocturnally active in the laboratory (Abello´ et al. 1991) and in the field at depths of 50–60 m (Patterson 1984). Undefined patterns of activity were reported in deeper areas at around 100 m (Trenkel et al. 2007). The ecological and behavioural aspects of M. intermedia and M. tenuimana are also poorly understood at present (Mori et al. 2004). Both species were classified as either epibenthic (Gramitto & Froglia 1998) or endobenthic (Hartnoll et al. 1992) with aggressive territorial behaviour (Attrill et al. 1990; Mori et al. 2004). However, observations of behavioural rhythms in other species of the genus Munida have provided contradictory results. For example, Munida sarsi is diurnal (Hudson & Wigham 2003), Munida rugosa is either diurnal (Nickell & Sayer 1998) or arrhythmic (Trenkel et al. 2007), and Munida bamffica is apparently nocturnal (Patterson 1984). A recent trawl survey reported a nocturnal increase in catches of M. tenuimana in different deep-water strata (from 700 to 1200 m; Sarda` et al. 2003). To date, studies focusing on behavioural rhythms of deep-water decapod crustaceans are scant (reviewed by 94
Aguzzi & Sarda` 2008). Data on the circadian behaviour of species (i.e. the autoecological perspective) are required to build an integrated model that accounts for changes in the structuring of marine communities over a 24-h cycle (i.e. the sinecological perspective). In this context, our aim is to measure behavioural rhythms of L. depurator, M. intermedia and M. tenuimana to identify their type of displacement (i.e. endobenthic, nektobenthic or benthopelagic). Also, it is not know whether modulations exist in their rhythmic behaviour due to gender or ontogeny, and we sought to investigate this possibility as well. A temporally scheduled series of trawl hauls was carried out close to the autumn equinox and the summer solstice at shelf depths of 100–110 m and slope depths of 400–430 m. Resulting catch patterns were used as a proxy of animal activity rhythms and examined in relation to the 24-h cycle and seasonal variation in photoperiod length. The contents of catches were also analysed with respect to the sex and size of the animals.
Material and Methods Species
In the western Mediterranean, Liocarcinus depurator is one of the dominant brachyuran species of the continental shelf (Abello´ et al. 1988, 2002; Fanelli et al. 2007). Its bathymetric distribution encompasses a wide depth range (i.e. 50–800 m; Abello´ et al. 2002; Rufino et al. 2005) with highest densities at around 50–100 m (Abello´ et al. 1988, 2002; Rufino et al. 2006). In the same area, Munida intermedia and M. tenuimana show a different bathymetric distribution. Munida intermedia is mainly distributed from the shelf-break to the middle slope, with abundance peaks between 120 and 800 m (Gramitto & Froglia 1998; Mori et al. 2004). In contrast, M. tenuimana mostly occur on the middle and lower slope (e.g. Abello´ et al. 1988, 2002), with the highest densities reported between 400 and 550 m (Huguet et al. 2005). Sampling
Two geographically close sites in the western Mediterranean were selected (Fig. 1): one on the lower continental shelf (100–110 m depth) off the Ebro delta (4039¢ N, 113¢ E; 4038¢ N, 111¢ E) and the other on the upper slope (400–430 m) off Tarragona (4101¢ N, 137¢ E; 4055¢ N, 131¢ E) (see also Aguzzi et al. 2003). Sampling was performed onboard the R ⁄ V Garcı´a del Cid (38 m length; 1200 HP) equipped with otter trawl gear whose vertical mouth opening was 1.4–1.6 m (OTMS, Sarda` et al. 1998). The net adheres to the seabed surface during the towing procedure and its mouth closes when the gear
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
Aguzzi, Company & Garcı´a
Behavioural rhythms of deep water crustacean decapods
12 h of day and 12 h of night) and from 22 June to 3 July 2000 (close to the summer solstice, with a 15-h day and 9-h night). Replicate trawl hauls were continuously carried out over four consecutive days at both depths, each for 3–4 h along parallel transects of similar length (4.7 ± 1.4 km) located at close proximity to each other (Fig. 1). A GPS system recorded the velocity of the ship and the initial and final positions for all hauls. These numbers are detailed in Table 1. The echo-sounder provided all depth measures. Trawl sensors (Scanmar) were connected to the net mouth to record the functioning and opening of the wings. Data were telemetrically stored on a computer onboard. Initial and final trawl timing was recorded by noting the exact time of the net landing and rising from the seabed. Light intensity cycles were measured as photon fluency rate (PFR, lEiÆm)2Æs)1) between wavelengths of 400 and 700 nm. Measures were taken between consecutive hauls with a photometer (LI-193SA Spherical Quantum Sensor) mounted on a CTD. Light levels on the upper slope were below the sensitivity range of the photometer and therefore illumination was only sampled in a direct manner down to 300 m depth. Light intensity at 400–430 m was then calculated according to Tobar & Sarda` (1992).
N
200 m Barcelona Tarragona 41°
1000 m
400 m 100 m
Ebro Delta
0°
1°
2°
E
Fig. 1. Study area off the Catalan coast (Western Mediterranean) showing sampling transects at 100–110 m and 400–430 m; 200 m and 1000 m isobaths are shown.
is lifted off the seabed, so that there is no chance of contamination of bottom catches with pelagic organisms (Sarda` et al. 1998). The trawl net does not dig into the substrate during the tow, so animals buried more than 5–10 cm in the substrate are not accessible to sampling (Aguzzi et al. 2003, 2006a). The coupling of behavioural rhythms with light intensity cycles of different amplitudes (i.e. depths) and photophase lengths (i.e. seasons) was assessed by repeating the sampling at 100–110 and 400–430 m from 28 September to 8 October 1999 (close to the autumn equinox, with
Table 1. Number of hauls and PFR readings used for mean density and light intensity estimations within each 2-h interval in the waveform analysis of the time series of data for Liocarcinus depurator, Munida intermedia and Munida tenuimana.
Catchability rhythms
The makeup of bottom catches is representative of the numbers of animals present on the seabed at the time of the haul (Aguzzi et al. 2003). Fluctuations in the makeup of trawl captures over a 24-h period can be used as a
no. hauls
no. PFR readings
October
June
October
June
time interval (h)
shelf
slope
shelf
slope
shelf
slope
shelf
slope
12–14 14–16 16–18 18–20 20–22 22–00 00–02 02–04 04–06 06–08 08–10 10–12
1 4 3 1 4 4 – 3 2 3 4 3
3 – 4 3 4 4 1 2 2 3 5 3
3 1 3 5 4 – 3 1 4 4 4 –
3 1 4 4 4 – 2 2 4 3 3 1
3 3 1 – n.p. n.p. n.p. n.p. n.p. 3 4 4
3 4 1 1 n.p. n.p. n.p. n.p. n.p. 4 3 3
– 1 2 4 n.p. n.p. n.p. n.p. 4 4 2 4
1 – 3 4 n.p. n.p. n.p. n.p. 2 3 2 3
Data are reported for samplings on the continental shelf (100 m depth) and upper slope (400 m) in October and June. n.p., nocturnal period, no light measurements were performed. –, no samples were collected at the corresponding time interval during the 4 days of sampling.
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
95
Aguzzi, Company & Garcı´a
Behavioural rhythms of deep water crustacean decapods
proxy measure of the rhythmic behaviour of bottomdwelling species (Reebs 2002). Consequently, the terms ‘catch’ and ‘density’ are used synonymously. For each haul, all individuals of L. depurator, M. intermedia and M. tenuimana were sorted, counted and sexed, and their carapace length (CL) was measured with a calliper (± 0.1 mm precision). A density value was obtained per haul by dividing the number of sampled animals of each species by the swept area (in km2) as estimated by Scanmar and GPS data (Sparre et al. 1989). For every sampled depth and season, density data were plotted as a function of the starting time of each haul (i.e. the time that the net landed as indicated by Scanmar sensors). The time of sunset and sunrise at the latitude under study (Greenwich Meridian Time: 17:39 and 05:44 hours on the 28 Oct; 19:27 and 04:19 hours on the 22 June) were also reported in the plots. The timing of activity peaks (i.e. the phase) was defined by waveform analysis on the time series of density values. The phase agreement with the light intensity cycle was measured by repeating waveform analysis on PFR values. Waveform analysis is currently used in chronobiology when behavioural data are examined (see Refinetti 2006 for a review on this methodology). In our case, it consisted of the subdivision of catch and PFR time series into 24-h segments whose values were averaged (± SD) at corresponding 2-h intervals (see Table 1). For those time intervals where no haul was performed or no light intensity was sampled (due to technical reasons), a mean (± SD) density or PFR was computed from the values of adjacent intervals (e.g. in Table 1, October at 400 m, the missing value of the interval 14–16 h was replaced by an average computed from all values of 12–14- and 16–18-h intervals, n = 3 and n = 4, respectively). In each waveform plot, the peak was identified by computing a threshold average from all of its values (i.e. daily mean; adapted from Hammond & Naylor 1977; see also Aguzzi et al. 2003). Values above that daily mean indicate the presence of a significant increase in catches. Peak limits (i.e. phase onset and offset) were identified by the first and last value above the daily mean. These limits were compared with the corresponding light intensity levels. Periodicity in the density data time series was screened between 9 and 30 h with a Chi-squared periodogram analysis (ClockLab Actimetrics, Evanston, IL, USA). This analysis requires that data were taken at constant time intervals. Gaps in the time series were therefore replaced by waveforms values of corresponding 2-h intervals (Aguzzi et al. 2003). In periodograms, the highest significant (P < 0.01) peak represented the maximum percentage of the total data variance fitted by the corresponding periodicity (see Refinetti 2006 for a review on this methodology); this peak value was chosen for period attribution. 96
To assess whether there were different behavioural rhythms for different sexes or sizes of animals, waveform and periodogram analyses were repeated separately on the time series for different demographic groups: males, females, juveniles and adults. To classify the animals by age, the following size-class limits were chosen: for L. depurator CL < 20 mm and CL > 20 mm (Abello´ 1989; Abello´ et al. 1990); for M. intermedia CL < 11 mm and CL > 11 mm (Company 1995; Gramitto & Froglia 1998; Mori et al. 2004); and finally, for M. tenuimana CL < 12 mm and CL > 12 mm (Company et al. 2003; Huguet et al. 2005). Results Catches of L. depurator increased markedly at night in October and June at 100–110 m (i.e. the shelf; Fig. 2a,b). Catchability patterns changed at 400–430 m (i.e. the slope; Fig. 2c,d), where peaks were bimodal, with a nocturnal and a diurnal peak. Comparing data at both depths, the range of fluctuation in catches varied by several orders of magnitude (e.g. in October, absolute maxima of 14 · 103 indÆkm)2 at the first day on the shelf; 160 indÆkm)2 at the third day on the slope). Repeating that comparison for both seasons, catch patterns at 100 m fluctuated in June over a range that was half of that reported in October. Conversely, at 400 m these ranges were almost similar. At 400 m, M. intermedia presented an undefined pattern of fluctuation in catches during October (Fig. 3a) and a bimodal pattern in June, with nocturnal and diurnal peaks (Fig. 3b). Catch fluctuation ranges were similar in both seasons (i.e. totals in captures of 53,694 indÆkm)2 in October to 50,511 indÆkm)2 in June). Catch patterns of M. tenuimana at 400 m had nocturnal and diurnal peaks that varied in amplitude over consecutive days in October (Fig. 3c). In June (Fig. 3d) that fluctuation dampened, but two major peaks were still recorded at night (i.e. in the first and the fourth day). A seasonal reduction in catches, to almost half, occurred from October to June (i.e. from totals in captures of 33,285 to 18,091 indÆkm)2). Waveform analysis was performed to define precisely the timing of catch pattern maxima (i.e. the phase of species’ behavioural activity) with respect to the light intensity cycle and the seasonal variation in the length of the photoperiod. Periodogram analysis was then carried out on simulated time series of catches to measure the occurrence of significant periodicity. Light intensity (i.e. PFR measures) decreased by several orders of magnitude from the shelf to the slope (e.g. in June in the time interval 10.00–12.00 h: from 2.5 ± 0.28 lEiÆm)2Æs)1 at 100 m to 9.2 · 10)8 ± 8.3 · 10)8 lEiÆm)2Æs)1 at 400 m).
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
Aguzzi, Company & Garcı´a
Behavioural rhythms of deep water crustacean decapods
11:30
5:30
23:30
17:30
5:30
11:30
23:30
17:30
23:30 21:00
11:30
17:30 15:00
5:30
5:30
11:30 9:00
23:30
3:00
7:00
1:00
19:00
7:00
13:00
1:00
19:00
0 13:00
0
1:00
10 7:00
20
20 19:00
40
7:00
30
13:00
60
1:00
40
19:00
50
80
13:00
100
21:00
60
June
17:30
120
102 no. km–2
100 m b 70
15:00
October a 140
400 m c 450
d 450
400
400 350
300
300 250
250 200
200 150
150 100
9:00
3:00
21:00
15:00
9:00
3:00
21:00
15:00
10:30
4:30
22:30
16:30
10:30
4:30
22:30
10:30
16:30
4:30
16:30
22:30
10:30
4:30
16:30
22:30
10:30
0
9:00
100 50 0
50
3:00
no. km–2
350
Time of day (h) Fig. 2. Catch patterns (density, nÆkm)2) reported for Liocarcinus depurator in October and June on the shelf (a,b; 100 m) and the slope (c,d; 400 m). Shaded vertical rectangles indicate the night duration.
At 100 m (Fig. 4a,b) L. depurator showed a marked early nocturnal phase in October, the onset and the offset of which were reported respectively at time intervals: 16:00–18:00 h and 0:00–2:00 h. In June, that phase was preserved, although its onset and offset moved according to the seasonal contraction of the scotophase 18:00–20:00 h and 02:00–04:00 h. Catch patterns at 100 m for both seasons presented a significant periodicity of 24 h. Considering the correlation between catch patterns and the light intensity cycle, phase onsets occurred for PFR values equal to 0.3 and 0.1 lEiÆm)2Æs)1 in October and June. In both seasons, the offset always anticipated the sunrise at light intensity levels equal to 0 lEiÆm)2Æs)1. For L. depurator at 400 m (Fig. 4c,d) the waveform analysis showed bimodal profiles with significant 12.1-h periodicity in both sampling seasons. In October (Fig. 4c) the first peak occurred immediately after sunset (onset and offset: 18:00–20:00 h; 20:00–22:00 h), and the second occurred at sunrise (onset and offset: 04:00–06:00 h; 08:00–10:00 h). In June (Fig. 4d), a similar but broader bimodal profile was reported (i.e. the sunset peak lasted from 18:00–20:00 h to 0:00–2:00 h; the diurnal peak onset and offset were centred at 08:00–10:00 h). Comparison with PFR data indicated that the first nocturnal increase
started below 3 · 10)8 lEiÆm)2Æs)1 in both seasons, while daytime maxima occurred for light values of 8 · 10)8 lEiÆm)2Æs)1 in October and 2 · 10)8 lEiÆm)2Æs)1 in June. The waveform analysis on M. intermedia time series at 400 m (Fig. 5a,b) indicated the occurrence of a broad diurnal fluctuation pattern in October. Periodogram analysis found a significant 24-h periodicity. In June, waveform analysis revealed the occurrence of a pronounced bimodal pattern of fluctuation in catches, created by an early scotophase peak (onset and offset: 18:00–20:00 h, below 1 · 10)9 lEiÆm)2Æs)1; 22:00–0:00 h) and a midday photophase peak (maximum at 2 · 10)8 lEiÆm)2Æs)1; onset and offset: 08:00–10:00 h; 12:00–14:00 h). Periodogram analysis indicated a 12-h significant periodicity. The waveform analysis on time series for M. tenuimana at 400 m (Fig. 5c,d) showed a marked bimodal pattern of fluctuation in October, with peaks phased at midnight and midday. As peak maxima were distributed at a time lag shorter than 12 h, arrhythmia was reported in periodogram analysis on simulated catch time series. For June, the waveform analysis reported a broad nocturnal peak (onset and offset: 18:00–20:00 h, below 2 · 10)9 lEiÆ m)2Æs)1; 04:00–06:00 h, above 1 · 10)9 lEiÆm)2Æs)1)
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
97
Aguzzi, Company & Garcı´a
Behavioural rhythms of deep water crustacean decapods
3:00
9:00
15:00
21:00
3:00
9:00
9:00
15:00
21:00
3:00
9:00
21:00 21:00
3:00
9:00
3:00 3:00
15:00
21:00 21:00
15:00
9:00
15:00 15:00
3:00
9:00
21:00
3:00
15.00
4:30
9:00
June
Munida intermedia b 50 40 35 30 25 20 15 10 5 0 10:30
22:30
16:30
4:30
10:30
22:30
16:30
4:30
10:30
22:30
16:30
10:30
4:30
16:30
10:30
102 no. km–2
22:30
October
a 50 40 35 30 25 20 15 10 5 0
15:00
4:30 10:30
22:30
16:30
10:30
0
4:30
0
22:30
5 16:30
5 10:30
10
4:30
10
22:30
15
16:30
15
10:30
20
4:30
20
22:30
25
16:30
25
10:30
d 30
21:00
Munida tenuimana
c 30
Time of day (h) Fig. 3. Catch patterns (density, nÆkm)2) reported on the slope (400 m) in October and June for Munida intermedia (a,b) and Munida tenuimana (c,d). Shaded vertical rectangles indicate the night duration.
accompanied by a weak diurnal increase (maximum at 12:00–14:00 h, for 6 · 10)8 lEiÆm)2Æs)1). Periodogram analysis indicated a significant 24-h periodicity. Waveform and periodogram analyses were repeated on time series of captures for males, females, juveniles and adults, to assess the occurrence of gender or ontogenetic modulations in species behavioural rhythms. In L. depurator at 100 m (Fig. 6a), males and females showed the same nocturnal phase in waveform analysis for October and June, with a significant 24-h periodicity in periodogram analysis. At 400 m, in October and June females showed a bimodal fluctuation in catches, with a 12.0-h significant periodicity. The waveform profiles for males displayed a similar bimodal pattern in June (significant periodicity of 12 h) but these were not discernible in October (detected as arrhythmic in periodogram analysis on simulated time series). In contrast, juveniles presented a bimodal catch pattern in waveform analysis for October to June with a significant 12.0-h periodicity. Peaks relative to temporal distance shortened from autumn to spring–summer. In contrast, adults showed a marked nocturnal increase in catches in both October and June. A significant 24-h periodicity was found in both seasons. 98
In L. depurator at 400 m catch patterns for both sexes and class sizes were less defined according to the reduction in the number of sampled individuals (see Fig. 2). Catch patterns for juveniles and adults were similarly bimodal in October (significant periodicity of 12 h). In June, adults preserved the bimodal fluctuation, while juveniles showed a single nocturnal increase in catches (i.e. significant periodicities of 12 and 24 h, respectively). For M. intermedia (Fig. 6b), in October, the analysis of catch patterns by sex showed no differences. Waveforms were equally unimodal in October (24-h periodicity) and bimodal in June (12-h periodicity). The analysis by size indicated similarities in behavioural patterns of juveniles and adults in June (a 12-h bimodal periodicity) but not in October, when juveniles were arrhythmic. For M. tenuimana (Fig. 6b), the catch patterns for males and females were similar in October, when arrhythmia in periodogram analysis was reported. Catch patterns were also similar in June where periodogram analysis showed a 24-h periodicity with a nocturnal peak in waveform analysis. Juveniles in October presented a 12-h periodicity with two peaks in waveform analysis. That pattern was not defined in adults, who conversely showed a waveform output with unclear phase and arrhythmia in periodogram
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
Aguzzi, Company & Garcı´a
Behavioural rhythms of deep water crustacean decapods
October
a 140 120 100 80 60 40 20
c
24.0 2.7 2.4 2.1 1.8 1.5 1.2 0.9 0.6 0.3 * 0.0 12 14 16 18 20 2 0 2 4 6 8 1 –1 –1 –1 –2 –2 2–0 –2 –4 –6 –8 –10 0–1 4 6 8 0 2 2
35 30 25 20 15 10 5 0
24.0 2.7 2.4 2.1 1.8 1.5 1.2 0.9 0.6 0.3 0.0 * * 6 2 2 1 4 0 8 12 14 16 18 20 –1 –1 –1 –2 –2 2–0 –2 –4 –6 –8 –10 0–1 6 2 8 0 2 4
400 m d 2.4
12.0
2.4
b 40
12.0
PFR (µEim–2s–1)
102 no. km–2
0
June
100 m
2.0–07
2.0–07
2.0
2.0 1.6
1.5–07
1.6
1.5–07
1.2
1.0–07
1.2
1.0–07
0.8
0.8 5.0–08
0.4 0
12
* 0 2 6 1 1 2 1 8 2 0 4 1 –1 4–1 6–1 8–2 0–2 2–0 –2 –4 –6 –8 –10 0–1 2 8 0 4 2 6
5.0–08
0.4 0
12
* 0 6 8 4 2 0 1 1 1 2 2 1 –1 4–1 6–1 8–2 0–2 2–0 –2 –4 –6 –8 –10 0–1 4 8 6 2 2 0
Time of day (h) Fig. 4. Waveform analysis (mean density, nÆkm)2 ± SD) on time series of catches for Liocarcinus depurator and PFR (i.e. light intensity) values in October and June on the shelf (a,b; 100 m) and the slope (c,d; 400 m). Periodogram analysis outputs are also reported as a measure of significant periodicity (in h) of simulated time series. Horizontal dashed lines are the mean density thresholds used to define peak timing and duration. At 100 m and 400 m, threshold values are: 6084 and 69 in October; 1358 and 94, in June. Black vertical arrows indicate the temporal limits as onset (upward) or offset (downward), of active phases in waveform plots. Missing density (*) and PFR (•) values for some time intervals were interpolated from adjacent measures (see Table 1).
analysis. In June the waveform analysis output for juveniles had no discernible pattern with arrhythmia in periodogram analysis. Adults were nocturnal in the waveform plot, and periodogram analysis detected a significant 24-h periodicity.
Discussion
the seabed (Herring & Roe 1988). Conversely, for endobenthic species, maxima in capture indicate the occurrence of an active phase, as animals increase their rate of motion to emerge from the substrate (Aguzzi et al. 2006a, 2007). Accordingly, the present catch data are analysed to characterize activity rhythms only after the type of displacement is defined for each species studied (see next sections).
General results
In this study, marked behavioural rhythms were reported for L. depurator, M. intermedia and M. tenuimana at different depths, and hence different light intensity regimes. Such rhythms were found by temporally scheduled trawling, an active method of sampling (Reebs 2002) that did not per se provide indications of the true timing in the active phase of species. Catch data need to be considered with respect to data on the different types of species’ displacement (Table 2). For example, peaks in catches (i.e. trawling) of benthopelagic species at the seabed are indicators of an inactive phase as these animals descend to rest and hide on
The behavioural rhythms of L. depurator
Field data (Figs 3 and 4) indicate that L. depurator is captured nocturnally at the shelf (100–110 m), as already observed for shallower areas (40–60 m; Patterson 1984). Abello´ et al. (1991) reported a marked nocturnal activity in laboratory tests with animals from 30 to 40 m depth. On the slope (400–430 m), animals display a bimodal capture pattern with activity peaks at midday and midnight. Liocarcinus depurator was classified as a benthopelagic (i.e. vertically moving) species (Johnson & Rees 1988),
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
99
Aguzzi, Company & Garcı´a
Behavioural rhythms of deep water crustacean decapods
October Arr.
a 30
2.0–07
12.0
b 30
2.0–07
25
25 20
1.5–07
20
1.5–07
15
1.0–07
15
1.0–07
10
10 5.0–08
5
*
0
2 –1 10 10 8– 8 6– 6 4– 4 2– 2 0– –0 22 2 –2 20 0 –2 18 8 –1 16 6 –1
0
–1 4
2 –1 10 10 8– 8 6– 6 4– 4 2– 2 0– –0 22 2 –2 20 0 –2 18 8 –1 16 6 –1 14 4 –1 12
12
14
102 no. km–2
0
5.0–08
5
Munida tenuimana Arr.
24.0
20
2.0–07 d 20
15
1.5–07
15
1.5–07
10
1.0–07
10
1.0–07
5
5.0–08
5
5.0–08
0
0
*
0
PFR (µEim–2s–1)
*
0
c
June
Munida intermedia
2.0–07
*
0
0
12
10–
8–1
6–8
4–6
2–4
0–2
14
0 22– 22 20– 20 18– 18 16– 16
14–
12–
12 10– 0
8–1
6–8
4–6
2–4
0–2
16
14
0 22– 22 20– 20 18– 18
16–
14–
12–
Time of day (h) Fig. 5. Waveform analysis (mean density, nÆkm)2 ± SD) on time series of PFR (i.e. light intensity) values and catches at 400 m reported in October and June for Munida intermedia (a,b) and Munida tenuimana (c,d). Periodogram analysis outputs are also reported as a measure of significant periodicity (in h) of simulated time series. Horizontal dashed lines are the mean density thresholds used to define peak timing and duration in the activity of M. intermedia (October 1542; June 1582) and M. tenuimana (October 953; June 592). Black vertical arrows indicate the temporal limits as onset (upward) or offset (downward), of active phases in waveform plots. Missing density (*) and PFR (•) values for some time intervals were interpolated from adjacent measures (see Table 1).
with the peculiar characteristic of hiding in the sediment when inactive (Hall et al. 1990). From our data, L. depurator disappears from daytime catches at 100–110 m. In this sense, it does not behave like the majority of benthopelagic species, which display nocturnal upward migratory activity, and are mostly captured by trawling in the day (Herring & Roe 1988). This would indicate that L. depurator is not a benthopelagic species. Other burying shrimps of the same depth and community such as Solenocera membranacea and Chlorotocus crassicornis hide in the sediment when inactive at daytime, and are captured in high numbers during the night when they actively emerge from the sediment. Their catchability patterns are similar to those reported here for L. depurator. These species do not perform benthopelagic vertical migration as Pasiphaea sivado and Pasiphaea multidentata do, for which no burying activity has been reported in the same area of this study and with a similar method and schedule of sampling (Cartes et al. 1993; Aguzzi et al. 2006b). In this scenario, we propose that L. depurator is an 100
endobenthic burying species. At 5–10 cm deep in the substrate, buriers can efficiently avoid trawl tow capture (Aguzzi et al. 2006a). Animals emerge from the sediment under the protection of the darkness (Freire et al. 1991) and are captured at night when crawling and swimming on the seabed to forage (Nickell & Moore 1992). This seems to be confirmed by other indirect observations. In decapods, feeding coincides with moments of behavioural activity. The depth levels where ingested preys move match those where predators are (e.g. Cartes 1993, 1995). Accordingly, stomach content analysis in L. depurator reveals that most prey items are associated with the bottom typical of benthic species and not with the upper layers of the water column as reported for benthopelagic movers (Thrush 1986; Hall et al. 1990; Freire 1996). In this study, a clear diel modulation of L. depurator behaviour was reported on the shelf. This was much weaker, and hence less defined, on the slope where animal densities are reduced. The analysis of slope data is still
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
Aguzzi, Company & Garcı´a
Behavioural rhythms of deep water crustacean decapods
October
Liocarcinus depurator
24.0 24.0
12.0 24.0
12.0 24.0
12.0 Arr.
12.0 12.0
12.0 12.0
24.0 12.0
12 10– 0 8–1 6–8 4–6 2–4 0–2 0 22– 22 20– 20 18– 18 16– 16 14– 14 12–
b
June
24.0 24.0
12 10– 0 8–1 6–8 4–6 2–4 0–2 0 22– 22 20– 20 18– 18 16– 16 14– 14 12–
Significant increase in catches
400 m
100 m
a
Munida intermedia 24.0 24.0
12.0 12.0
Arr. 24.0
12.0 12.0
Munida tenuimana Arr. Arr.
24.0 24.0
12.0 Arr.
Arr. 24.0
2 –1 10 0 1 8– 8 6– 6 4– 4 2– 2 0– –0 22 2 –2 20 20 – 18 8 –1 16 16 – 14 14 – 12
2 –1 10 0 1 8– 8 6– 6 4– 4 2– 2 0– –0 22 2 –2 20 0 –2 18 18 – 16 6 –1 14 14 – 12
Time of day (h) Fig. 6. Waveform and periodogram analyses on time series of catches of Liocarcinus depurator at 100 m and 400 m (a) and Munida intermedia and Munida tenuimana at 400 m (b) sorted by sex and size, in October and June. To facilitate the phase comparisons, the peak temporal amplitude (i.e. as values in mean catches above the daily mean) are reported as horizontal bars (females – grey, males – black, juveniles – white, and adults – thick black). Shaded vertical rectangles indicate the night duration.
useful to describe the circadian modulation of behaviour in species with wide bathymetric distribution ranges, that are hence experiencing light intensity cycles of a markedly different amplitude. In the study area, a decrease in light intensity of seven orders of magnitude was reported when moving from 100 to 400 m depth (Fig. 4). Accordingly, the expression of diel rhythmic behaviour in L. depurator weakens and the amplitude of catch patterns decreases with an increase of the bathymetry of sampling. From a strong nocturnal activity rhythm at 100 m (i.e. 24-h significant periodicity), a bimodal periodicity with nocturnal and diurnal peaks is reported at 400 m (i.e. 12-h significant periodicity). At this depth, animals were
active on the seabed for longer periods of time in comparison with the shelf, staying emerged after sunrise (Fig. 4). On the shelf, L. depurator starts its behavioural activity suddenly at sunset, but catches decrease gradually over the following hours, with the majority of animals hidden in the substrate well before dawn. Laboratory data on endogenous swimming rhythm in L. depurator suggest a similar nocturnal behavioural activity (Abello´ et al. 1991). Unfortunately, the absence of waveform analysis in this laboratory study does not allow for the comparison between the behavioural performances of single animals (i.e. from the laboratory) and populations (present field
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
101
Aguzzi, Company & Garcı´a
Behavioural rhythms of deep water crustacean decapods
Table 2. Different types of displacement (endobenthic-burrowers and -buriers; nektobenthic and benthopelagic) are compared with predictions on species’ behavioural activity based on reported catchability patterns over the 24 h (i.e. peaks or troughs). Trawl catch data Typology of displacement
peaks
troughs
species
source
burrowers
activity
inactivity
buriers
activity
inactivity
nektobenthic
activitya
inactivitya
benthopelagic
inactivity
activity
Nephrops norvegicus; Goneplax rhomboides; Squilla mantis Solenocera membranacea; Chlorotocus crassicornis; Processa canaliculata Plesionika gigliolii; Plesionika martia; Aristaeus antennatus Pasiphaea sivado; Pasiphaea multidentata
Atkinson 1974; Froglia & Giannini 1989; Aguzzi et al. 2003, 2006a, 2007 Froglia & Gramitto 1987; Aguzzi et al. 2006a, 2007, 2008 Tobar & Sarda` 1992; Cartes et al. 1993; Aguzzi et al. 2007 Cartes et al. 1993; Aguzzi et al. 2006b
This classification was based on previously published data for decapod species of the Mediterranean area, the references of which are also reported. a It should be noted that for nektobenthic species, trawling peaks coincide with phases of behavioural activity only when the sampling is performed at the upper limit of their bathymetric displacement.
results). A similar progressively decreasing activity after sunset was reported in other burying species of the same area at the same depth (e.g. S. membranacea; Aguzzi et al. 2006a). Possibly, burying crabs emerge at the onset of darkness to perform behavioural activity of ecological importance (e.g. feeding) protected from visual predators by the darkness (McGaw 2005). The fatigue or the accomplishment of their tasks determines their subsequent reburying, well before the end of the darkness phase (Aguzzi et al. 2006a). Ontogenetic (i.e. size-related) differences were found in the rhythmic behaviour of L. depurator at both sampling depths. At 100 m, we captured a larger number of juveniles at sunset and sunrise. Their activity rhythm has a 12h periodicity (Fig. 6a). Conversely, adults were present on the seabed only at nighttime. These data are in agreement with other field reports. Feeding data account for marked ontogenetic, but not gender, differences in selected prey items (Abello´ & Cartes 1987; Freire 1996). Also, Liocarcinus displays aggressive intra-specific competition often resulting in cannibalism (Hall et al. 1990). Most of the fights are initiated spontaneously by opponents irrespective of their size, but the fights are always won by the larger crab (Glass & Huntingford 1988; Huntingford et al. 1995). The reported size modulation of emergence behaviour may be caused by intra-specific competition between juveniles and adults. In areas of high density (i.e. present data from 100 m), the anticipation at sunset and the delay at sunrise of the emergence of juveniles may occur because these juveniles avoid adults during the night. The same analysis on the slope (400 m), where reported densities are lower, revealed a superposition in the activity phase (i.e. catches) of both demographic groups in October but not in June (Fig. 6a). In June, a slight increase in recorded abundances occurs due to a change in juvenile behavioural 102
rhythms, suggesting that modulation of behaviour due to density occurs in a similar fashion to that observed on the shelf. Adults are active on the seabed for longer periods of time including the daytime, while juveniles confine their activity to only the scotophase. The behavioural rhythms of M. intermedia and M. tenuimana
In this study, M. intermedia and M. tenuimana showed fluctuations of significant periodicity in catches at slope (400 m). Both species were classified as either endobenthic-borrowers (Hartnoll et al. 1992) or epibenthic (i.e. generally staying on the seabed) with or without partial burying or burrowing activity (Gramitto & Froglia 1998). Deducing behavioural activity in epibenthic species from temporally scheduled trawling often produces indiscernible patterns in catch time series. Animals are available for sampling irrespective of the phase of their behavioural activity, and laboratory tests are needed for comparison with field data when their rhythmic biology has to be characterized (reviewed by Aguzzi & Sarda` 2008). In this study, we reported fluctuations in catches that, given the low motility of squat lobsters (Company & Sarda` 1998; Maynou & Cartes 1998), cannot be attributed to bathymetric nektobenthic displacements (i.e. causing drops in catches when animals move at other seabed depths). Catch fluctuations are then an indication of a burying activity, as animals are unavailable for trawl capture when hiding a few centimetres deep in the sediment. During emergence, animals roam (but not swim; Company & Sarda` 1998) in the surrounding seabed areas to forage on detritus (Cartes et al. 2007) or perform active predation on natantian decapods present in the benthic boundary layer (Hudson & Wigham 2003; Cartes & Maynou 1998).
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
Aguzzi, Company & Garcı´a
In this study, M. intermedia were weakly diurnal in October, and both diurnal and nocturnal in June (significant 12-h periodicity; Fig. 5a,b). In contrast, M. tenuimana presented no discernible rhythmicity in October, limiting its emergence to hours of darkness in June (Fig. 5c,d). In that season, animals emerged during the second half of the night, whereas for M. intermedia this occurred in the first half. These data suggest that interspecific competition modulates the behavioural activity rhythm of both species when these co-occur (Huguet et al. 2005). This modulation is the basis of their temporal partitioning of access to similar ecological resources, allowing their co-existence into the same area (Kornfeld-Schor & Dayan 2003). The succession of several species of the genus Munida over a depth gradient indicates the occurrence of some degree of habitat partitioning among them. Apparently, such partitioning is not based on feeding resources, given the wide diet spectrum of these species (Huguet et al. 2005). Possibly, the M. tenuimana and M. intermedia territorial behaviour (Attrill et al. 1990; Mori et al. 2004) forces animals of both species to share the same seabed at different hours of the day. Neither species presented evident sex or size modulations in their emergence behaviour. The absence of size modulation in the activity rhythms of Munida spp. is a typical feature of the endobenthos. Animals are equally protected from visual predators when hiding in the sediment, irrespective of their size (Aguzzi & Sarda` 2008). Comparing the present results for M. tenuimana with those of Sarda` et al. (2003) in deep water areas (700–1200 m), catch patterns, and hence activity rhythms, maintain a broad nocturnal phase down to the twilight zone (at around 1000 m depth in the Mediterranean; Margalef 1977). If M. tenuimana care considered a proxy for other species with no displacement, then animals are influenced by light throughout their depth range. If behavioural rhythms are light-driven, photic entrainment occurs in animal responses to fluctuations in the local environmental light at a wavelength close to 480 nm (i.e. blue light). Such a high energy frequency is the only one present over the whole depth range of oceanic photic zones (Jerlov 1968). Acknowledgements The authors wish to thank F. Sarda`, Chief Investigator of the project NERIT (MAR98-0935) funded by the Spanish CICYT and the crew of the R ⁄ V Garcı´a del Cid (CSIC) for their support during sampling. Special thanks are also given to P. Abello´, B. Molı´ and A. Castello´n for their valuable technical help during sampling operations. J. Aguzzi is a Post-doctoral fellow in the Juan de la Cierva Program.
Behavioural rhythms of deep water crustacean decapods
References Abello´ P. (1989) Reproduction and moulting of Liocarcinus depurator (Linnaeus, 1758) (Brachyura: Portunidae) in the northwestern Mediterranean Sea. Scientia Marina, 53, 117–124. Abello´ P., Cartes J.E. (1987) Observations on the diet of Liocarcinus depurator (L.) (Brachyura: Portunidae) in the Catalan Sea. Investigacio´n Pesqueras, 51 (Suppl. 1), 413–419. Abello´ P., Valladares F.J., Castello´n A. (1988) Analysis of the structure of decapod crustacean assemblages off the Catalan coast (North-West Mediterranean). Marine Biology, 98, 39–49. Abello´ P., Pertierra J.P., Reid D.G. (1990) Sexual size dimorphism, relative growth and handedness in Liocarcinus depurator and Macropipus tuberculatus (Brachyura: Portunidae). Scientia Marina, 54, 195–202. Abello´ P., Reid D.G., Naylor E. (1991) Comparative locomotor activity patterns in the portunid crabs Liocarcinus holsatus and L. depurator. Journal of the Marine Biological Association of the UK, 71, 1–10. Abello´ P., Carbonell A., Torres P. (2002) Biogeography of epibenthic crustaceans on the shelf and upper slope off the Iberian Peninsula Mediterranean coasts: implications for the establishment of natural management areas. Scientia Marina, 66 (Suppl. 2), 183–198. Aguzzi J., Sarda` F. (2008). A history of recent advancements on Nephrops norvegicus behavioural and physiological rhythms. Review of Fish Biology and Fisheries, 18, 235–248. Aguzzi J., Sarda` F., Abello´ P., Company J.B., Rotllant G. (2003) Diel and seasonal patterns of Nephrops norvegicus (Decapoda: Nephropidae) catchability in the Western Mediterranean. Marine Ecology Progress Series, 258, 201–211. Aguzzi J., Company J.B., Abello´ P., Garcı´a J.A. (2006a) Rhythmic behaviour of the burying prawn Solenocera membranacea (Decapoda: Penaeoidea: Solenoceridae) in the Western Mediterranean: a perspective through depth and season. Bulletin of Marine Science, 79, 353–364. Aguzzi J., Company J.B., Abello´ P., Garcı´a J.A. (2006b) Ontogenetic changes in the vertical migratory rhythms of benthopelagic shrimps Pasiphaea multidentata and P. sivado (Crustacea: Caridea). Marine Ecology Progress Series, 335, 167–174. Aguzzi J., Company J.B., Abello´ P., Garcı´a J.A. (2007) Rhythmic diel movements of some pandalid shrimps (Decapoda: Caridea) in the western Mediterranean continental shelf and upper slope. Journal of Zoology, 273, 340–349. Aguzzi J., Company J.B., Garcı´a J.A. (2008). The circadian behavioural regulation of the shrimp, Processa canaliculata Leach, 1815 (Processidae) in relation to depth, ontogeny, and the reproductive cycle. Crustaceana (in press). Atkinson R.J.A. (1974) The activity rhythm of Goneplax rhomboides (L.). Marine Behavioural Physiology, 2, 325–335. Attrill M.J., Hartnoll R.G., Rice A.L., Thurston M.H. (1990) A depth-related distribution of the red crab, Geryon
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
103
Behavioural rhythms of deep water crustacean decapods
trispinosus (Herbst) [= G. tridens Kroyer]: indications of vertical migration. Progress in Oceanography, 24, 197–206. Bellwood O. (2002) The occurrence, mechanics and significance of burying behaviour in crabs (Crustacea: Brachyura). Journal of Natural History, 36, 1223–1238. Cartes J.E. (1993) Day-night feeding by decapods crustaceans in a deep-water bottom community in the Western Mediterranean. Journal of the Marine Biological Association of the UK, 73, 795–811. Cartes J.E. (1995) Diets of, and trophic resources exploited by, bathyal penaeoidean shrimps from the Western Mediterranean. Marine and Freshwater Research, 46, 889–996. Cartes J.E., Maynou F. (1998) Food consumption by bathyal decapod crustacean assemblages in the Western Mediterranean: An approach to predatory impact by megafauna and to a food consumption-food supply balance in a deep-water food web. Marine Ecology Progress Series, 171, 233–246. Cartes J.E., Sarda` F., Company J.B., Llenorat J. (1993) Daynight migrations by deep-sea decapod crustaceans in experimental samplings in the Western Mediterranean sea. Journal of Experimental Marine Biology and Ecology, 171, 63–73. Cartes J., Huguet C., Parra S., Sanchez F. (2007) Trophic relationships in deep-water decapods of Le Danois bank (Cantabrian Sea, NE Atlantic): Trends related with depth and seasonal changes in food quality and availability. Deep-Sea Research I, 54, 1091–1110. Company J.B. (1995). Estudi comparatiu de les estrate`gies biolo`giques dels crustacis deca`podes del talu´s de la Mar Catalana. Ph.D. thesis, University of Barcelona, 130 pp. Company J.B., Sarda` F. (1998) Metabolic rates and energy content of deep-sea benthic decapod crustaceans in the Western Mediterranean Sea. Deep-Sea Research I, 45, 1861–1880. Company J.B., Sarda` F., Puig P., Cartes J.E., Palanques A. (2003) Duration and timing of reproduction in decapod crustaceans of the NW Mediterranean continental margin: is there a general pattern? Marine Ecology Progress Series, 261, 201–216. Fanelli E., Cartes J.E. (2004) Feeding habits of pandalid shrimps in the Alboran Sea (SW Mediterranean): influence of biological and environmental factors. Marine Ecology Progress Series, 280, 227–238. Fanelli E., Colloca F., Ardizzone G. (2007) Decapod crustacean assemblages off the west coast of Central Italy (Western Mediterranean). Scientia Marina, 71, 19–28. Freire J. (1996) Feeding ecology of Liocarcinus depurator (Decapoda: Portunidae) in the Rı´a de Arousa (Galicia, NW Spain): Effects of habitat, season and life history. Marine Biology, 126, 297–311. Freire J., Ferna´ndez L., Gonza´lez-Gurriara´n E. (1991) Diel feeding pattern of Liocarcinus depurator (Brachyura: Portunidae) in the Rı´a de Arousa (Galicia, NW Spain). Ophelia, 33, 165–177. Froglia C., Giannini S. (1989). Field observations on diel rhythms in catchability and feeding of Squilla mantis (L.) (Crustacea, Stomatopoda) in the Adriatic Sea. In: Ferrero
104
Aguzzi, Company & Garcı´a
E.A. (Ed.), Biology of the Stomatopods. Mucchi, Modena: 221–228. Froglia C., Gramitto E. (1987) Notes on growth and biology of Solenocera membranacea (Risso, 1816) in the Central Adriatic Sea (Decapoda: Solenoceridae). Investigacı´on. Pesqueras, 51(1), 189–199. Glass C.W., Huntingford F.A. (1988) Initiation and resolution of fights between swimming crabs (Liocarcinus depurator). Ethology, 77, 237–249. Gramitto M.E., Froglia C. (1998) Notes on the biology and growth of Munida intermedia (Anomura: Galatheidae) in the western Pomo Pit. Journal of Natural History, 32, 1553– 1566. Hall S.J., Raffaelli D., Robertson M.R., Basford D.J. (1990) The role of the predatory crab, Liocarcinus depurator in the marine food web. Journal of Animal Ecology, 59, 421–438. Hammond R.D., Naylor E. (1977) Effects of dusk and down on locomotor activity rhythms in the Norway lobster Nephrops norvegicus. Marine Biology, 39, 253–260. Hartnoll R.G., Rice A.L., Attrill M.J. (1992) Aspects of the biology of the galatheid genus Munida (Crustacea, Decapoda) from the Porcupine Seabight, Northeast Atlantic. Sarsia, 76, 231–246. Herring P.J., Roe H.S.J. (1988) The photoecology of pelagic oceanic decapods. Symposium of the Zoological Society of London, 59, 263–290. Hudson I.R., Wigham B.D. (2003) In situ observations of the predatory feeding behaviour of the galatheid squat lobster Munida sarsi using a remotely operated vehicle. Journal of the Marine Biological Association of the UK, 83, 463–464. Huguet C., Maynou F., Abello´ P. (2005) Small scale distribution characteristics of Munida spp. populations (Decapoda: Anomura) off the Catalan coasts (Western Mediterranean). Journal of Sea Research, 53, 283–296. Huntingford F.A., Taylor A.C., Smith I.P., Thorpe K.E. (1995) Behavioural and physiological studies of aggression in swimming crabs. Journal of Experimental Marine Biology and Ecology, 193, 21–39. Jerlov N.G. (1968) Optical Oceanography. Elsevier, Amsterdam. Johnson L., Rees C.J.C. (1988) Oxygen consumption and gill surface area in relation to habitat and lifestyle of four crab species. Comparative Biochemistry and Physiology, 89A, 243–246. Kronfeld-Schor N., Dayan T. (2003) Partitioning of time as an ecological resource. Annual Review of Ecology, Evolution and Systematic, 34, 153–181. Margalef R. (1977). Ecologı´a. Omega Ed., S. A., Barcelona, 951 pp. Maynou F.X., Cartes J.E. (1998) Daily ration estimates and comparative study of food consumption in nine species of deep-water decapod crustaceans of the NW Mediterranean. Marine Ecology Progress Series, 171, 221–231. McGaw I. (2005) Burying behaviour of two sympatric crab species: Cancer magister and Cancer productus. Scientia Marina, 69, 375–381.
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
Aguzzi, Company & Garcı´a
Moreno-Amich M.R. (1994) Feeding habits of the grey gurnard, Eutrigla gurnardus (L., 1758) along the Catalan coast (Northwestern Mediterranean). Hydrobiologia, 273, 57–66. Mori M., Sbrana M., Sartor P., De Ranieri S. (2004) Aspetti bio-ecologici di Munida intermedia (Crustacea, Decapoda, Anomura) nell’arcipelago Toscano meridionale (Tirreno settentrionale). Atti della Societa´ Toscana di Scienze Naturali, Memorie Serie B, 111, 43–53. Naylor E. (1985) Tidally rhythmic behaviour of marine animals. Symposia of the Society for Experimental Biology, 39, 63–93. Naylor E. (2005) Chronobiology: implications for marine resources exploitation and management. Scientia Marina, 69 (Suppl.1), 157–167. Nickell T.D., Moore P.G. (1992) The behavioural ecology of epibenthic scavenging invertebrates in the Clyde Sea area: laboratory experiments on attractions to bait in moving water, underwater TV observations in situ and general conclusions. Marine Ecology Progress Series, 159, 15–35. Nickell L.A., Sayer M.D.J. (1998) Occurrence and activity of mobile macrofauna on a sublittoral reef: diel and seasonal variation. Journal of the Marine Biological Association of the UK, 78, 1061–1082. Patterson K.R. (1984) Distribution patterns of some epifauna in the Irish Sea and their ecological interactions. Marine Biology, 83, 103–108. Pittman S.J., McAlpine C.A. (2001) Movements of marine fish and decapods crustaceans: process, theory and application. Advances in Marine Biology, 44, 206–295. Reebs S.G. (2002) Plasticity of diel and circadian activity rhythms in fishes. Review of Fish Biology and Fisheries, 12, 349–371. Refinetti R. (2006). Circadian Physiology, 2nd edition. Taylor & Francis, Boca Raton. Rufino M., Abello´ P., Yule A., Torres P. (2005) Geographic, bathymetric and inter-annual variability in the distribution
Behavioural rhythms of deep water crustacean decapods
of Liocarcinus depurator (Brachyura: Portunidae) along the Mediterranean coast of Iberian Peninsula. Scientia Marina, 69, 503–518. Rufino M., Maynou F., Abello´ P., Yule A., Gil de Sola L. (2006) Geostatistical analysis of densities of Liocarcinus depurator (Brachyura: Portunidae) on the Western Mediterranean from 1994 to 2003. Marine Biology, 149, 855–864. Sarda` F., Cartes J.E., Company J.B., Antoni A. (1998) A modified commercial trawl used to sample deep-sea megabenthos. Fisheries Science, 64, 492–493. Sarda` F., Company J.B., Castello´n A. (2003) Intraspecific aggregation structure of a shoal of Western Mediterranean (Catalan coast) deep-sea shrimp, Aristeus antennatus (Risso, 1816), during the reproductive period. Journal of Shellfish Research, 22, 569–579. Sparre P., Ursin E., Vemena S.C. (1989). Introduction to Tropical Fish Stock Assessment Part 1. FAO Fisheries Technical Paper 306 ⁄ 1. FAO, Rome. Thrush S.F. (1986) Community structure in the floor of the sea-lough: are large epibenthic predators important? Journal of Experimental Marine Biology and Ecology, 104, 171–183. Tobar R., Sarda` F. (1992) Annual and diel light intensity cycle as a predictive factor in deep-water fisheries for the prawn Aristeus antennatus Risso, 1816. Fisheries Research, 15, 179– 196. Trenkel V.M., Le Loch F., Rochet M.J. (2007) Small scale spatial and temporal interactions among benthic crustaceans and one fish species in the Bay of Biscay. Marine Biology, 151, 2207–2215. Yamaguchi A., Tsutomu I., Watanabe Y., Ishizaka J. (2004) Vertical distribution patterns of pelagic copepods as viewed from the predation pressure hypothesis. Zoological Studies, 43, 475–485.
Marine Ecology 30 (2009) 93–105 ª 2008 The Authors. Journal compilation ª 2008 Blackwell Publishing Ltd
105
