Abstract
Light is the most important zeitgeber for the synchronization of biological rhythms in terrestrial organisms. In the sea, the light intensity progressively decreases, and tidal currents might control behavioural rhythms at disphotic depths. The Norway lobster, Nephrops norvegicus, is distributed from the upper shelf to middle slope areas. Its burrowing behaviour is under the control of a circadian system, and the effects of tidal currents have been inferred from catchability patterns. Male lobsters were collected from 100 m depth off the Ebro Delta, Tarragona, Spain (40° 39′N, 1° 13′E). Light intensity and water current cycles were simulated in the laboratory to investigate their combined effects on burrow emergence behavioural rhythms (June–July 2012). Periodic water currents (10 cm s−1) inhibited N. norvegicus burrow emergence to a degree dependent on the relative phase between light and water current cycles. The lobsters preferred to remain inside the burrow in the presence of water currents. However, when they were outside the burrow, they spent more time orientated downstream during darkness hours. Moreover, four of the 15 lobsters showed that a current could act as a putative zeitgeber for the circadian oscillator, but further experiments are needed to confirm this finding. These results indicate that tidal current is an important parameter to consider when interpreting fishery-dependent data and data from video surveys, not only N. norvegicus, but for other deep-water epibenthic species.
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References
Aguzzi J, Company JB (2010) Chronobiology of deep-water decapod crustaceans on continental margins. Adv Mar Biol 58:155–225. doi:10.1016/B978-0-12-381015-1.00003-4
Aguzzi J, Sardà F (2008) A history of recent advancements on Nephrops norvegicus behavioral and physiological rhythms. Rev Fish Biol Fish 18:235–248. doi:10.1007/s11160-007-9071-9
Aguzzi J, Sarriá D, García JA, Del Rio J, Sardà F, Manuel A (2008) A new tracking system for the measurement of diel locomotor rhythms in the Norway lobster, Nephrops norvegicus (L.). J Neurosci Methods 173:215–224. doi:10.1016/j.jneumeth.2008.06.009
Aguzzi J, Costa C, Furushima Y, Chiesa JJ, Menesatti P, Iwase R, Fujiwara Y (2010) Behavioral rhythms of hydrocarbon seep fauna in relation to internal tides. Mar Ecol Prog Ser 418:47–56
Aguzzi J, Company JB, Costa C, Menesatti P, Garcia JA, Bahamon N, Puig P, Sarda F (2011) Activity rhythms in the deep-sea: a chronobiological approach. Front Biosci (Landmark Ed) 16:131–150
Aguzzi J, Sbragaglia V, Tecchio S, Navarro J, Company JB (2015) Rhythmic behaviour of marine benthopelagic species and the synchronous dynamics of benthic communities. Deep Sea Res Pt I 95:1–11. doi:10.1016/j.dsr.2014.10.003
Arnold G (1981) Movements of fish in relation to water currents. In: Aidley D (ed) Animal migration. Cambridge University Press, Cambridge, pp 55–79
Arnold GP, Walker MG, Emerson LS, Holford BH (1994) Movements of cod (Gadus morhua L.) in relation to the tidal streams in the southern North Sea. ICES J Mar Sci 51:207–232. doi:10.1006/jmsc.1994.1021
Atkinson RJA, Naylor E (1976) An endogenous activity rhythm and the rhythmicity of catches of Nephrops norvegicus (L). J Exp Mar Biol Ecol 25:95–108. doi:10.1016/0022-0981(76)90079-4
Bell MC, Redant F, Tuck I (2006) Nephrops Species. In: Phillips B (ed) Lobsters: biology, management, aquaculture and fisheries. Blackwell, Oxford, pp 412–461
Bell MC, Elson JM, Addison JT, Revill AS, Bevan D (2008) Trawl catch composition in relation to Norway lobster (Nephrops norvegicus L.) abundance on the Farn Deeps grounds, NE England. Fish Res 90:128–137. doi:10.1016/j.fishres.2007.10.003
Breithaupt T, Tautz J (1990) The sensitivity of crayfish mechanoreceptors to hydrodynamic and acoustic stimuli. In: Wiese K, Krenz WD, Tautz J, Reichert H, Mulloney B (eds) Frontiers in crustacean neurobiology. Birkhäuser, Basel, pp 114–120
Chapman C (1980) Ecology of juvenile and adult Nephrops. In: Cobb J, Phillips B (eds) The biology and management of lobsters. Academic Press, New York, pp 143–178
Chiesa JJ, Aguzzi J, García JA, Sardà F, de la Iglesia HO (2010) Light intensity determines temporal niche switching of behavioral activity in deep-water Nephrops norvegicus (Crustacea: Decapoda). J Biol Rhythm 25:277–287. doi:10.1177/0748730410376159
Dunlap JC, Loros JJ, DeCoursey PJ (2004) Chronobiology: biological timekeeping. Sinauer Associates, Sunderland
Farmer A (1975) Synopsis of biological data on the Norway lobster Nephrops norvegicus (Linnaeus, 1758). FAO Fish Synop 112:1–97
Fernández De Miguel F, Aréchiga H (1994) Circadian locomotor activity and its entrainment by food in the crayfish Procambarus clarkii. J Exp Biol 190:9–21
Fraser PJ, Cruickshank SF, Shelmerdine RL (2003) Hydrostatic pressure effects on vestibular hair cell afferents in fish and crustacea. J Vestibul Res Equilib 13:235–242
Gibson RN (1992) Tidally-synchronised behaviour in marine fishes. In: Ali MA (ed) Rhythms in fishes. Springer, New York, pp 63–81
Hammond R, Naylor E (1977) Effects of dusk and dawn on locomotor activity rhythms in the Norway lobster Nephrops norvegicus. Mar Biol 39:253–260
Hillis JP (1971) Studies on Dublin Bay prawns (Nephrops norvegicus) in the Irish Sea. Fish Leafl Dep Mar 22:1–11
Hillis JP (1996) Factors affecting catchability in Nephrops: current speed. ICES CM K:21
Hopkins TS (1985) Physics of the sea. In: Margalef R (ed) Key environments: Western Mediterranean. Pergamon Press, New York, pp 100–125
Johnson ML, Johnson MP (2013) The ecology and biology of Nephrops norvegicus. Academic Press, Adv Mar Biol 64
Johnson MP, Lordan C, Power AM (2013) Habitat and ecology of Nephrops norvegicus. In: Johnson ML, Johnson MP (eds) The ecology and biology of Nephrops norvegicus. Adv Mar Biol. Academic Press 64:27–63
Katoh E, Sbragaglia V, Aguzzi J, Breithaupt T (2013) Sensory biology and behaviour of Nephrops norvegicus. In: Johnson ML, Johnson MP (eds) The ecology and biology of Nephrops norvegicus. Adv Mar Biol. Academic Press 64: 65–106
Koehl MA (2011) Hydrodynamics of sniffing by crustaceans. In: Breithaupt T, Thiel M (eds) Chemical communication in crustaceans. Springer, Berlin, pp 85–102
Krumme U (2009) Diel and tidal movements by fish and decapods linking tropical coastal ecosystems. In: Nagelkerken I (ed) Ecological connectivity among tropical coastal ecosystems. Springer, Netherlands, pp 271–324
Krumme U, Saint-Paul U, Rosenthal H (2004) Tidal and diel changes in the structure of a nekton assemblage in small intertidal mangrove creeks in northern Brazil. Aquat Living Resour 17:215–229. doi:10.1051/alr:2004019
Laroche J, Baran E, Rasoanandrasana N (1997) Temporal patterns in a fish assemblage of a semiarid mangrove zone in Madagascar. J Fish Biol 51:3–20
Last KS, Bailhache T, Kramer C, Kyriacou CP, Rosato E, Olive PJW (2009) Tidal, daily, and lunar-day activity cycles in the marine polychaete Nereis virens. Chronobiol Int 26:167–183. doi:10.1080/07420520902774524
Loc’h FL, Hily C (2005) Stable carbon and nitrogen isotope analysis of Nephrops norvegicus/Merluccius merluccius fishing grounds in the Bay of Biscay (Northeast Atlantic). Can J Fish Aquat Sci 62:123–132
Lorance P, Trenkel VM (2006) Variability in natural behaviour, and observed reactions to an ROV, by mid-slope fish species. J Exp Mar Biol Ecol 332:106–119
Main J, Sangster GI (1985) The behaviour of the Norway lobster Nephrops norvegicus (L.), during trawling. Scott Fish Res Rep 34:1–23
Maltagliati F, Camilli L, Biagi F, Abbiati M (1998) Genetic structure of Norway lobster, Nephrops norvegicus (L.) (Crustacea: Nephropidae), from the Mediterranean Sea. Sci Mar 62:91–99. doi:10.3989/scimar.1998.62s191
Michalsen K, Godø OR, Fernö A (1996) Diel variation in the catchability of gadoids and its influence on the reliability of abundance indices. ICES J Mar Sci 53:389–395
Mrosovsky N (1999) Masking: history, definitions, and measurement. Chronobiol Int 16:415–429
Naylor E (2010) Chronobiology of marine organisms. Cambridge University Press, Cambridge
Newland P, Chapman C (1989) The swimming and orientation behaviour of the Norway lobster, Nephrops norvegicus (L.), in relation to trawling. Fish Res 8:63–80
Newland P, Neil D, Chapman C (1988) The reactions of the Norway lobster, Nephrops norvegicus (L.), to water currents. Mar FreshW Behav Phy 13:301–313
Passamonti M, Mantovani B, Scali V, Froglia C (1997) Allozymic characterization of Scottish and Aegean populations of Nephrops norvegicus. J Mar Biol Assoc 77:727–735
Pinnegar JK, Platts M (2011) APSTOM—an integrated database and portal for fish stomach record. Version 3.6. Centre for Environment, Fisheries and Aquaculture Science, Lowestoft, UK. Phase 3, Final Report, July 2011
Refinetti R (2006) Circadian physiology, 2nd edn. Fla, CRC Press, Boca Raton
Refinetti R (2012) Integration of biological clocks and rhythms. Compr Physiol 2:1213–1239. doi:10.1002/cphy.c100088
Rice AL (1964) Observations on the effects of changes of hydrostatic pressure on the behaviour of some marine animals. J Mar Biol Assoc 44:163–175
Sbragaglia V, Aguzzi J, García J, Sarriá D, Gomariz S, Costa C, Menesatti P, Vilaró M, Manuel A, Sardà F (2013a) An automated multi-flume actograph for the study of behavioral rhythms of burrowing organisms. J Exp Mar Biol Ecol 446:177–185
Sbragaglia V, Aguzzi J, Garcia JA, Chiesa JJ, Angelini C, Sardà F (2013b) Dusk but not dawn burrow emergence rhythms of Nephrops norvegicus (Crustacea: Decapoda). Sci Mar 77:641–647
Schmitz OJ, Grabowski JH, Peckarsky BL, Preisser EL, Trussell GC, Vonesh JR (2008) From individuals to ecosystem function: toward an integration of evolutionary and ecosystem ecology. Ecology 89:2436–2445
Serrano A, Velasco F, Olaso I, Sánchez F (2003) Macrobenthic crustaceans in the diet of demersal fish in the Bay of Biscay in relation to abundance in the environment. Sarsia 88:36–48
Sokolove PG, Bushell WN (1978) The Chi square periodogram: its utility for analysis of circadian rhythms. J Theor Biol 72:131–160
Stamatis C, Triantafyllidis A, Moutou K, Mamuris Z (2004) Mitochondrial DNA variation in Northeast Atlantic and Mediterranean populations of Norway lobster, Nephrops norvegicus. Mol Ecol 13:1377–1390
Stewart JE, Horner GW, Arie B (1972) Effects of temperature, food, and starvation on several physiological parameters of the lobster Homarus americanus. J Fish Res Board Can 29:439–442. doi:10.1139/f72-072
Storrow B (1912) The prawn (Norway lobster, Nephrops norvegicus), and the prawn fishery of North Shields. Rep Dove Mar Lab 1:10–31
Thomas HJ (1965) The white-fish communities associated with Nephrops norvegicus (L.) and the by-catch of white fish in the Norway lobster fishery, together with notes on Norway lobster predators. Rapp. p.-v. réun. - Cons. int. explor. mer 156:155–160
Wagner H-J, Kemp K, Mattheus U, Priede I (2007) Rhythms at the bottom of the deep sea: cyclic current flow changes and melatonin patterns in two species of demersal fish. Deep Sea Res Pt I 54:1944–1956
Watson W, Chabot CC (2010) High resolution tracking of adult horseshoe crabs Limulus polyphemus in a New Hampshire estuary using a fixed array ultrasonic telemetry. Curr Zool 56:599–610
Wiese K (1976) Mechanoreceptors for near-field water displacements in crayfish. J Neurophysiol 39:816–833
Acknowledgments
This work is supported by the RITFIM project (CTM2010-16274; PI: J. Aguzzi) funded by the Ministry of Science and Innovation (MICINN). We are grateful to Dr. S. Tecchio (Normandie Université UNICAEN, UMR BOREA MNHN, UPMC, CNRS-7208, IRD-207) for his help in developing the smoothing functions applied in Fig. 3. We are also grateful to J. Grassle, I. G. Priede and another unknown reviewer for their help to improve the quality of the manuscript. VS is a Predoctoral Fellow within the Formation Personal Investigator (FPI) scheme (MICINN). JA is a Ramón y Cajal Programme (MICINN) Postdoctoral Fellow.
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The authors declare the absence of conflict of interests for the data presented in this paper. Sampling and laboratory experiments followed the local legislation regarding animal welfare.
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Sbragaglia, V., García, J.A., Chiesa, J.J. et al. Effect of simulated tidal currents on the burrow emergence rhythms of the Norway lobster (Nephrops norvegicus). Mar Biol 162, 2007–2016 (2015). https://doi.org/10.1007/s00227-015-2726-5
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DOI: https://doi.org/10.1007/s00227-015-2726-5