Extreme roll angles in Argentine sea bass: Could refuge ease posture and buoyancy control of marine coastal fishes?

Abstract

The swim bladder provides a mechanism for buoyancy regulation in teleosts. However, in certain species, its location can result in an unstable body position, with associated energetic costs assumed for maintaining posture in addition to the energetic demands from swim bladder volume regulation. Direct observations show that some body-compressed, cave-refuging teleosts that nominally operate near neutral buoyancy may adopt unusual body attitudes within crevices. We hypothesize that these fishes may relax their buoyancy and posture control mechanisms during periods of rest. A prediction derived from this is that resting fish may adopt a wide range of roll angles (i.e., rotation about their longitudinal axis) inside caves. To quantify this behavior and for testing this hypothesis, triaxial accelerometers were deployed on free-living, cave-refuging Argentine sea bass Acanthistius patachonicus, and the relationship between roll angle and a proxy for activity (defined as the vectorial dynamic body acceleration, VeDBA) was analyzed. The results were compared with data available for three other species of fishes with disparate body forms and lifestyles: the pelagic whale shark Rhincodon typus, the dorsoventrally compressed benthic great sculpin Myoxocephalus polyacanthocephalus, and the fusiform and demersal Atlantic cod Gadus morhua. Inactive Argentine sea bass adopted a wide variety of roll angles, including extreme ones exceeding 80°, but had lower roll angles closer to an upright posture primarily associated with higher activity levels. In contrast, the great sculpin and Atlantic cod both rested at a close to upright roll angle but had higher activity levels associated with larger roll angles. Whale shark did not rest for the duration of the recorded period and also showed higher activity levels associated with larger roll angles. We propose that relaxation of buoyancy and posture control may help to reduce the metabolic rate in laterally compressed, cave-refuging fishes during periods of rest within crevices.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Alexander RM (1990) Size, speed and buoyancy adaptations in aquatic animals. Am Zool 30:189–196

    Article  Google Scholar 

  2. Alexander RM (2002) Stability and manoeuvrability of terrestrial vertebrates. ICB 42:158–164

    Google Scholar 

  3. Anderson TW (2001) Predator responses, prey refuges, and density-dependent mortality of a marine fish. Ecology 82:245–257

    Article  Google Scholar 

  4. Blake RW (1979) The energetics of hovering in the mandarin fish (Synchropus picturatus). J Exp Biol 82:25–33

    Google Scholar 

  5. Broell F, Noda T, Wright S, Domenici P, Steffensen JF, Auclair J-P, Taggart CT (2013) Accelerometer tags: detecting and identifying activities in fish and the effect of sampling frequency. J Exp Biol 216:1255–1264

    Article  Google Scholar 

  6. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  7. Brownscombe JW, Gutowsky LFG, Danylchuk AJ, Cooke SJ (2014) Foraging behaviour and activity of a marine benthivorous fish estimated using tri-axial accelerometer biologgers. Mar Ecol Progr Ser 505:241–251

    Article  Google Scholar 

  8. Dellatorre FG, Pisoni JP, Barón PJ, Rivas AL (2012) Tide and wind forced nearshore dynamics in Nuevo Gulf (Northern Patagonia, Argentina): potential implications for cross-shore transport. J Mar Syst 96:82–89

    Article  Google Scholar 

  9. Eidietis L, Forrester TL, Webb PW (2002) Relative abilities to correct rolling disturbances of three morphologically different fish. Can J Zool 80:2156–2163

    Article  Google Scholar 

  10. Evans JR, Allen RM, Chung AI, Cochran ES, Guy R, Hellweg M, Lawrence JF (2014) Performance of several low cost accelerometers. Seismol Res Lett 85:147–158

    Article  Google Scholar 

  11. Galván DE, Parma AM, Iribarne O (2008) Influence of predatory reef fishes on the spatial distribution of Munida gregaria (=M. subrugosa) (Crustacea; Galatheidae) in shallow Patagonian soft bottoms. J Exp Mar Biol Ecol 354:93–100

    Article  Google Scholar 

  12. Galván DE, Venerus LA, Irigoyen AJ (2009a) The reef-fish fauna of the northern Patagonian gulfs, Argentina, southwestern Atlantic. Open Fish Sci J 2:90–98

    Article  Google Scholar 

  13. Galván DE, Botto F, Parma AM, Bandieri L, Mohamed N, Iribarne OO (2009b) Food partitioning and spatial subsidy in shelter-limited fishes inhabiting patchy reefs of Patagonia. J Fish Biol 75:2585–2605

    Article  Google Scholar 

  14. Gannon R, Taylor MD, Suthers IM, Gray CA, van der Meulen DE, Smith JA, Payne NL (2014) Thermal limitation of performance and biogeography in a free-ranging ectotherm: insights from accelerometry. J Exp Biol 217:3033–3037

    Article  Google Scholar 

  15. Gerstner CL (1998) Use of substratum ripples for flow refuging by Atlantic cod, Gadus morhua. Environ Biol Fishes 51:455–460

    Article  Google Scholar 

  16. Gleiss AC, Dale JJ, Holland KN, Wilson RP (2010) Accelerating estimates of activity-specific metabolic rate in fishes: testing the applicability of acceleration data-loggers. J Exp Mar Biol Ecol 385:85–91

    Article  Google Scholar 

  17. Gleiss AC, Wilson RP, Shepard ELC (2011) Making overall dynamic body acceleration work: on the theory of acceleration as a proxy for energy expenditure. Methods Ecol Evol 2:23–33

    Article  Google Scholar 

  18. Gleiss AC, Wright S, Liebsch N, Wilson RP, Norman B (2013) Contrasting diel patterns in vertical movement and locomotor activity of whale sharks at Ningaloo Reef. Mar Biol 160:2981–2992

    CAS  Article  Google Scholar 

  19. Gleiss AC, Potvin J, Keleher JJ, Whitty JM, Morgan DL, Goldbogen JA (2015) Mechanical challenges to freshwater residency in sharks and rays. J Exp Mar Biol. doi:10.1242/jeb.114868

    Google Scholar 

  20. Gruber SH, Nelson DR, Morrissey JF (1988) Patterns of activity and space utilization of lemon sharks, Negaprion brevirostris, in a shallow Bahamian lagoon. Bull Mar Sci 43:61–76

    Google Scholar 

  21. Grundy E, Jones MW, Laramee RS, Wilson RP, Shepard ELC (2009) Visualisation of sensor data from animal movement. In: Computer graphics forum. Wiley Online Library, p 815–822

  22. Halsey LG, Shepard ELC, Quintana F, Gomez Laich A, Green JA, Wilson RP (2009) The relationship between oxygen consumption and body acceleration in a range of species. Comp Bioch Physiol Part A Mol Integr Physiol 152:197–202

    CAS  Article  Google Scholar 

  23. Halsey LG, Matthews PGD, Rezende EL, Chauvaud L, Robson AA (2015) The interactions between temperature and activity levels in driving metabolic rate: theory, with empirical validation from contrasting ectotherms. Oecologia 177(4):1117–1129

    CAS  Article  Google Scholar 

  24. Hanson PC, Johnson TB, Schindler DE, Kitchell JF (1997) Fish Bioenergetics 3.0. University of Wisconsin Sea Grant Institute, WISCU-T-97-001, Madison, Wisconsin

  25. Helfman G, Collette BB, Facey DE, Bowen BW (2009) The diversity of fishes: biology, evolution, and ecology. Wiley, New York

    Google Scholar 

  26. Hixon MA, Beets JP (1993) Predation, prey refuges, and the structure of coral-reef fish assemblages. Ecol Monogr 63:77–101

    Article  Google Scholar 

  27. Irigoyen AJ, Venerus LA (2008) The pole-hooking method: a novel and economical technique for in situ tagging small to medium-sized fishes. Fish Res 91:349–353

    Article  Google Scholar 

  28. Irigoyen A, Cavaleri Gerhardinger L, Carvalho-Filho A (2008) On the status of the species of Acanthistius (Gill, 1862) (Percoidei) in the South-West Atlantic Ocean. Zootaxa 1813:51–59

    Google Scholar 

  29. Irigoyen AJ (2010) Efecto del alga invasora Undaria pinnatifida sobre la comunidad de peces de arrecife en los golfos Norpatagónicos. Ph.D. Thesis, University of Comahue

  30. Irigoyen AJ, Galván DE, Venerus LA, Parma AM (2013) Variability in abundance of temperate reef fishes estimated by visual Census. PLoS ONE 8:e61072

    CAS  Article  Google Scholar 

  31. Manly BFJ (1991) Randomization and Monte Carlo Methods in Biology. Chapman and Hall, London, UK, p 281

  32. McCutcheon FH (1966) Pressure sensitivity, reflexes, and buoyancy responses in teleosts. Anim Behav 14:204–217

    CAS  Article  Google Scholar 

  33. Mcnab BK (2002) The physiological ecology of vertebrates: a view from energetics. Cornell University Press, New York

    Google Scholar 

  34. Mehner T (2012) Diel vertical migration of freshwater fishes–proximate triggers, ultimate causes and research perspectives. Freshw Biol 57:1342–1359

    Article  Google Scholar 

  35. Perry RI, Smith SJ (1994) Identifying habitat associations of marine fishes using survey data: an application to the Northwest Atlantic. Can J Fish Aquat Sci 51:589–601

    Article  Google Scholar 

  36. Priede IG (1977) Natural selection for energetic efficiency and the relationship between activity level and mortality. Nature 267:610–611

    CAS  Article  Google Scholar 

  37. Qasem L, Cardew A, Wilson A, Griffiths I, Halsey LG, Shepard ELC, Gleiss AC, Wilson R (2012) Tri-axial dynamic acceleration as a proxy for animal energy expenditure; should we be summing values or calculating the vector? PLoS ONE 7:e31187

    CAS  Article  Google Scholar 

  38. R Development Core Team (2011) R: a language and environment for statistical computing. In: Computing RFfS (ed), Vienna, Austria

  39. Rubinich JP (2001) Edad y crecimiento del mero Acanthistius brasilianus (Pisces, Serranidae) en el golfo San Matías, Argentina. Universidad Nacional de la Patagonia San Juan Bosco, Puerto Madryn

    Google Scholar 

  40. Shasteen SP, Sheehan RJ (1997) Laboratory evaluation of artificial swim bladder deflation in largemouth bass: potential benefits for catch-and-release fisheries. N Am J Fish Manag 17:32–37

    Article  Google Scholar 

  41. Shepard ELC, Wilson RP, Halsey LG, Quintana F, Laich AG, Gleiss AC, Liebsch N, Myers AE, Norman B (2008a) Derivation of body motion via appropriate smoothing of acceleration data. Aquat Biol 4:235–241

    Article  Google Scholar 

  42. Shepard ELC, Wilson RP, Quintana F, Laich AG, Liebsch N, Albareda DA, Halsey LG, Gleiss A, Morgan DT, Myers AE (2008b) Identification of animal movement patterns using tri-axial accelerometry. Endang Species Res 10(2):1

    Google Scholar 

  43. Speers-Roesch B, Lingwood D, Stevens ED (2004) Effects of temperature and hydrostatic pressure on routine oxygen uptake of the bloater (Coregonus hoyi). J Gt Lakes Res 30:70–81

    CAS  Article  Google Scholar 

  44. Steele MA (1999) Effects of shelter and predators on reef fishes. J Exp Mar Biol Ecol 233:65–79

    Article  Google Scholar 

  45. Strand E, Jørgensen C, Huse G (2005) Modelling buoyancy regulation in fishes with swim bladders: bioenergetics and behaviour. Ecol Model 185:309–327

    Article  Google Scholar 

  46. Venerus LA, Irigoyen AJ, Galván DE, Parma AM (2014) Spatial dynamics of the Argentine sandperch, Pseudopercis semifasciata (Pinguipedidae), in temperate rocky reefs from northern Patagonia, Argentina. Mar Fresh Res 65:39–49

    Google Scholar 

  47. Webb PW (2002) Control of posture, depth, and swimming trajectories of fishes. ICB 42:94–101

    Google Scholar 

  48. Webb PW, Weihs D (1994) Hydrostatic stability of fish with swim bladders: not all fish are unstable. Can J Zool 72:1149–1154

    Article  Google Scholar 

  49. Webb PW, Weihs D (2015) Stability versus maneuvering challenges for stability during swimming by fishes. Integr Comp Biol. doi:10.1093/icb/icv053

    Google Scholar 

  50. Williams TM, Wolfe L, Davis T, Kendall T, Richter B, Wang Y, Bryce C, Elkaim GH, Wilmers CC (2014) Instantaneous energetics of puma kills reveal advantage of felid sneak attacks. Science 346:81–85

    CAS  Article  Google Scholar 

  51. Wilson RP, Shepard ELC, Liebsch N (2008) Prying into the intimate details of animal lives: use of a daily diary on animals. Endang Species Res 4:123–137

    Article  Google Scholar 

  52. Wright S, Metcalfe JD, Wilson R, Hetherington S (2014) Estimating activity-specific energy expenditure in a teleost fish, using accelerometer loggers. Mar Ecol Prog Ser 496:19–32

    Article  Google Scholar 

Download references

Acknowledgments

We want to thank P. Dell’Arciprete for her help with data analysis. This research was funded by Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT PICT 2010-203) and CONICET (PIP 11220110100634), both granted to JEC and The Explorer Club granted to L. Beltramino. B. Sheiko translated some paragraphs from the Russian literature on cottids. F. Broell, T. Noda, P. Domenici, J. Steffensen, J. Johansen, and J. Metcalfe helped with the experiments and provided data for great sculpin and Atlantic cod. P. Webb provided relevant criticism to an earlier version of the draft.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Javier E. Ciancio.

Additional information

Reviewed by Undisclosed experts.

Responsible Editor: G.H. Engelhard.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 10951 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ciancio, J.E., Venerus, L.A., Trobbiani, G.A. et al. Extreme roll angles in Argentine sea bass: Could refuge ease posture and buoyancy control of marine coastal fishes?. Mar Biol 163, 90 (2016). https://doi.org/10.1007/s00227-016-2869-z

Download citation

Keywords

  • Roll Angle
  • Triaxial Accelerometer
  • Whale Shark
  • Buoyancy Control
  • Reef Ledge