Diel patterns in swimming behavior of a vertically migrating deepwater shark, the bluntnose sixgill (Hexanchus griseus)

English version

Autoři: Daniel M. Coffey ^aff001; Mark A. Royer ^aff001; Carl G. Meyer ^aff001; Kim N. Holland ^aff001
Působiště autorů: Hawai‘i Institute of Marine Biology, University of Hawai‘i at Mānoa, Kāne‘ohe, Hawai‘i, United States of America ^aff001
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0228253

Souhrn

Diel vertical migration is a widespread behavioral phenomenon where organisms migrate through the water column and may modify behavior relative to changing environmental conditions based on physiological tolerances. Here, we combined a novel suite of biologging technologies to examine the thermal physiology (intramuscular temperature), fine-scale swimming behavior and activity (overall dynamic body acceleration as a proxy for energy expenditure) of bluntnose sixgill sharks (Hexanchus griseus) in response to environmental changes (depth, water temperature, dissolved oxygen) experienced during diel vertical migrations. In the subtropical waters off Hawai‘i, sixgill sharks undertook pronounced diel vertical migrations and spent considerable amounts of time in cold (5–7°C), low oxygen conditions (10–25% saturation) during their deeper daytime distribution. Further, sixgill sharks spent the majority of their deeper daytime distribution with intramuscular temperatures warmer than ambient water temperatures, thereby providing them with a significant thermal advantage over non-vertically migrating and smaller-sized prey. Sixgill sharks exhibited relatively high rates of activity during both shallow (night) and deep (day) phases and contrary to our predictions, did not reduce activity levels during their deeper daytime distribution while experiencing low temperature and dissolved oxygen levels. This demonstrates an ability to tolerate the low oxygen conditions occurring within the local oxygen minimum zone. The novel combination of biologging technologies used here enabled innovative in situ deep-sea natural experiments and provided significant insight into the behavioral and physiological ecology of an ecologically important deepwater species.

Klíčová slova:

Animal migration – Body temperature – Dissolved oxygen – Hidden Markov models – Oxygen – Oxygen metabolism – Sharks – Swimming

Zdroje

1. Neilson JD, Perry RI. Diel vertical migrations of marine fishes: an obligate or facultative process? Advances in Marine Biology. 1990;26:115–68. doi: 10.1016/s0065-2881(08)60200-x

2. Hays GC. A review of the adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Hydrobiologia. 2003;503:163–70.

3. Scheuerell MD, Schindler DE. Diel vertical migration by juvenile sockeye salmon: empirical evidence for the antipredation window. Ecology. 2003;84(7):1713–20.

4. Sims DW, Southall EJ, Tarling GA, Metcalfe JD. Habitat-specific normal and reverse diel vertical migration in the plankton-feeding basking shark. Journal of Animal Ecology. 2005;74(4):755–61.

5. Mehner T. Diel vertical migration of freshwater fishes—proximate triggers, ultimate causes and research perspectives. Freshwater Biology. 2012;57(7):1342–59.

6. Carey FG, Robison BH. Daily patterns in the activities of swordfish, Xiphias gladius, observed by acoustic telemetry. Fishery Bulletin. 1981;79(2):277–92.

7. Holland KN, Brill RW, Chang RKC, Sibert JR, Fournier DA. Physiological and behavioural thermoregulation in bigeye tuna (Thunnus obesus). Nature. 1992;358:410–2. doi: 10.1038/358410a0 1641023

8. Gilly WF, Zeidberg LD, Booth JA, Stewart JS, Marshall G, Abernathy K, et al. Locomotion and behavior of Humboldt squid, Dosidicus gigas, in relation to natural hypoxia in the Gulf of California, Mexico. The Journal of experimental biology. 2012;215(18):3175–90.

9. Nakamura I, Goto Y, Sato K. Ocean sunfish rewarm at the surface after deep excursions to forage for siphonophores. Journal of Animal Ecology. 2015;84(3):590–603. doi: 10.1111/1365-2656.12346 25643743

10. Comfort CM, Weng KC. Vertical habitat and behaviour of the bluntnose sixgill shark in Hawaii. Deep Sea Research Part II: Topical Studies in Oceanography. 2015;115:116–26.

11. Nakamura I, Meyer CG, Sato K. Unexpected positive buoyancy in deep sea sharks, Hexanchus griseus, and a Echinorhinus cookei. PloS one. 2015;10(6):e0127667. doi: 10.1371/journal.pone.0127667 26061525

12. Coffey DM, Holland KN. First autonomous recording of in situ dissolved oxygen from free-ranging fish. Animal Biotelemetry. 2015;3:47.

13. Vaquer-Sunyer R, Duarte CM. Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences. 2008;105(40):15452–7.

14. Ekau W, Auel H, Pörtner HO, Gilbert D. Impacts of hypoxia on the structure and processes in pelagic communities (zooplankton, macro-invertebrates and fish). Biogeosciences. 2010;7(5):1669–99.

15. Hofmann AF, Peltzer ET, Walz PM, Brewer PG. Hypoxia by degrees: establishing definitions for a changing ocean. Deep Sea Research Part I: Oceanographic Research Papers. 2011;58(12):1212–26.

16. Yeh J, Drazen JC. Depth zonation and bathymetric trends of deep-sea megafaunal scavengers of the Hawaiian Islands. Deep Sea Research Part I: Oceanographic Research Papers. 2009;56(2):251–66.

17. Childress JJ, Seibel BA. Life at stable low oxygen levels: adaptations of animals to oceanic oxygen minmum layers. Journal of Experimental Biology. 1998;201(8):1223–32.

18. Seibel BA. Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. Journal of Experimental Biology. 2011;214(2):326–36.

19. Huey RB, Kingsolver JG. Evolution of thermal sensitivity of ectotherm performance. Trends in Ecology & Evolution. 1989;4(5):131–5.

20. Dell AI, Pawar S, Savage VM. Systematic variation in the temperature dependence of physiological and ecological traits. Proceedings of the National Academy of Sciences. 2011;108(26):10591–6.

21. Payne NL, Smith JA, van der Meulen DE, Taylor MD, Watanabe YY, Takahashi A, et al. Temperature dependence of fish performance in the wild: links with species biogeography and physiological thermal tolerance. Functional Ecology. 2016;30(6):903–12.

22. Dell AI, Pawar S, Savage VM. Temperature dependence of trophic interactions are driven by asymmetry of species responses and foraging strategy. Journal of Animal Ecology. 2014;83(1):70–84. doi: 10.1111/1365-2656.12081 23692182

23. Sims DW, Wearmouth VJ, Southall EJ, Hill JM, Moore P, Rawlinson K, et al. Hunt warm, rest cool: bioenergetic strategy underlying diel vertical migration of a benthic shark. Journal of Animal Ecology. 2006;75(1):176–90. doi: 10.1111/j.1365-2656.2005.01033.x 16903055

24. Papastamatiou YP, Watanabe YY, Bradley D, Dee LE, Weng K, Lowe CG, et al. Drivers of daily routines in an ectothermic marine predator: hunt warm, rest warmer? PloS one. 2015;10(6):e0127807. doi: 10.1371/journal.pone.0127807 26061229

25. Neill WH, Stevens ED, Carey FG, Lawson KD, Mrosovsky N, Frair W. Thermal inertia versus thermoregulation in "warm" turtles and tunas. Science. 1974;184(4140):1008–10. doi: 10.1126/science.184.4140.1008 4826167

26. Neill WH, Chang RKC, Dizon AE. Magnitude and ecological implications of thermal inertia in skipjack tuna, Katsuwonus pelamis (Linnaeus). Environmental Biology of Fishes. 1976;1(1):61–80.

27. Wurtsbaugh WA, Neverman D. Post-feeding thermotaxis and daily vertical migration in a larval fish. Nature. 1988;333(6176):846–8.

28. Di Santo V, Bennett WA. Is post-feeding thermotaxis advantageous in elasmobranch fishes? Journal of Fish Biology. 2011;78(1):195–207. doi: 10.1111/j.1095-8649.2010.02853.x 21235555

29. Ebert DA. Some observations on the reproductive biology of the sixgill shark Hexanchus griseus (Bonnaterre, 1788) from southern African waters. African Journal of Marine Science. 2002;24:359–63.

30. Ebert DA, editor Aspects on the biology of hexanchoid sharks along the California coast. Second International Conference on Indo-Pacific Fishes; 1986; Tokyo: Ichthyological Society of Japan.

31. Nelson DR, McKibben JN, Strong WR, Lowe CG, Sisneros JA, Schroeder DM, et al. An acoustic tracking of a megamouth shark, Megachasma pelagios: a crepuscular vertical migrator. Environmental Biology of Fishes. 1997;49(4):389–99.

32. Holland KN, Sibert JR. Physiological thermoregulation in bigeye tuna. Environmental Biology of Fishes. 1994;40(3):319–27.

33. Sakamoto KQ, Sato K, Ishizuka M, Watanuki Y, Takahashi A, Daunt F, et al. Can ethograms be automatically generated using body acceleration data from free-ranging birds? PloS one. 2009;4(4):e5379. doi: 10.1371/journal.pone.0005379 19404389

34. Collins PM, Green JA, Warwick-Evans V, Dodd S, Shaw PJ, Arnould JP, et al. Interpreting behaviors from accelerometry: a method combining simplicity and objectivity. Ecology and Evolution. 2015;5(20):4642–54. doi: 10.1002/ece3.1660 26668729

35. Kawatsu S, Sato K, Watanabe Y, Hyodo S, Breves JP, Fox BK, et al. A New Method to Calibrate Attachment Angles of Data Loggers in Swimming Sharks. EURASIP Journal on Advances in Signal Processing. 2010;2010:732586.

36. Nakamura I, Watanabe YY, Papastamatiou YP, Sato K, Meyer CG. Yo-yo vertical movements suggest a foraging strategy for tiger sharks Galeocerdo cuvier. Marine Ecology Progress Series. 2011;424:237–46.

37. Wilson RP, White CR, Quintana F, Halsey LG, Liebsch N, Martin GR, et al. Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant. Journal of Animal Ecology. 2006;75(5):1081–90. doi: 10.1111/j.1365-2656.2006.01127.x 16922843

38. Halsey LG, Shepard EL, Quintana F, Gomez Laich A, Green JA, Wilson RP. The relationship between oxygen consumption and body acceleration in a range of species. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 2009;152(2):197–202.

39. Gleiss AC, Wilson RP, Shepard ELC. Making overall dynamic body acceleration work: on the theory of acceleration as a proxy for energy expenditure. Methods in Ecology and Evolution. 2011;2(1):23–33.

40. Qasem L, Cardew A, Wilson A, Griffiths I, Halsey LG, Shepard EL, et al. Tri-axial dynamic acceleration as a proxy for animal energy expenditure; should we be summing values or calculating the vector? PloS one. 2012;7(2):e31187. doi: 10.1371/journal.pone.0031187 22363576

41. Zuur AF, Ieno EN, Elphick CS. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution. 2010;1(1):3–14.

42. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. Mixed Effects Models and Extensions in Ecology with R. Gail M, Krickeberg K, Samet JM, Tsiatis A, Wong W, editors. New York, NY: Springer; 2009. 574 p.

43. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2018.

44. Wood SN, Scheipl F, Faraway JJ. Straightforward intermediate rank tensor product smoothing in mixed models. Statistics and Computing. 2013;23(3):341–60.

45. Wood SN. Generalized Additive Models: An Introduction with R. Second ed. Boca Raton, FL: CRC Press; 2017.

46. Burnham KP, Anderson DR. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. 2nd ed. New York, NY: Springer; 2002. 496 p.

47. Langrock R, King R, Matthiopoulos J, Thomas L, Fortin D, Morales JM. Flexible and practical modeling of animal telemetry data: hidden Markov models and extensions. Ecology. 2012;93(11):2336–42. doi: 10.1890/11-2241.1 23236905

48. Leos-Barajas V, Photopoulou T, Langrock R, Patterson TA, Watanabe YY, Murgatroyd M, et al. Analysis of animal accelerometer data using hidden Markov models. Methods in Ecology and Evolution. 2017;8(2):161–73.

49. Patterson TA, Basson M, Bravington MV, Gunn JS. Classifying movement behaviour in relation to environmental conditions using hidden Markov models. Journal of Animal Ecology. 2009;78(6):1113–23. doi: 10.1111/j.1365-2656.2009.01583.x 19563470

50. Papastamatiou YP, Watanabe YY, Demsar U, Leos-Barajas V, Bradley D, Langrock R, et al. Activity seascapes highlight central place foraging strategies in marine predators that never stop swimming. Movement Ecology. 2018;6:9. doi: 10.1186/s40462-018-0127-3 29951206

51. Gleiss AC, Norman B, Wilson RP. Moved by that sinking feeling: variable diving geometry underlies movement strategies in whale sharks. Functional Ecology. 2011;25(3):595–607.

52. Gleiss AC, Gruber SH, Wilson RP. Multi-channel data-logging: towards determination of behaviour and metabolic rate in free-swimming sharks. In: Nielsen JL, Arrizabalaga H, Fragoso N, Hobday A, Lutcavage M, Sibert J, editors. Tagging and Tracking of Marine Animals with Electronic Devices. Reviews: Methods and Technologies in Fish Biology and Fisheries. 9. Dordrecht, Netherlands: Springer; 2009. p. 211–28.

53. McClintock BT, Michelot T. momentuHMM: R package for generalized hidden Markov models of animal movement. Methods in Ecology and Evolution. 2018;9(6):1518–30.

54. Zucchini W, MacDonald IL, Langrock R. Hidden Markov Models for Time Series: An Introduction Using R. Second ed. Boca Raton, FL: CRC Press; 2016.

55. Grassmann M, McNeil B, Wharton J. Sharks in captivity: the role of husbandry, breeding, education, and citizen science in shark conservation. In: Larson SE, Lowry D, editors. Northeast Pacific Shark Biology, Research and Conservation Part B. Advances in Marine Biology. 78: Academic Press; 2017. p. 89–119.

56. Carey FG, Clark E. Depth telemetry from the sixgill shark, Hexanchus griseus, at Bermuda. Environmental Biology of Fishes. 1995;42(1):7–14.

57. Andrews KS, Levin PS, Katz SL, Farrer D, Gallucci VF, Bargmann G. Acoustic monitoring of sixgill shark movements in Puget Sound: evidence for localized movement. Canadian Journal of Zoology. 2007;85(11):1136–43.

58. Andrews KS, Williams GD, Farrer D, Tolimieri N, Harvey CJ, Bargmann G, et al. Diel activity patterns of sixgill sharks, Hexanchus griseus: the ups and downs of an apex predator. Animal Behaviour. 2009;78(2):525–36.

59. King JR, Surry AM. Seasonal and daily movements of the bluntnose sixgill shark (Hexanchus griseus) in the strait of Georgia from satellite tag data. Environmental Biology of Fishes. 2017;100(12):1543–59.

60. Rodríguez-Cabello C, González-Pola C, Rodríguez A, Sánchez F. Insights about depth distribution, occurrence and swimming behavior of Hexanchus griseus in the Cantabrian Sea (NE Atlantic). Regional Studies in Marine Science. 2018;23:60–72.

61. Gleiss AC, Wright S, Liebsch N, Wilson RP, Norman B. Contrasting diel patterns in vertical movement and locomotor activity of whale sharks at Ningaloo Reef. Marine Biology. 2013;160(11):2981–92.

62. Gleiss AC, Morgan DL, Whitty JM, Keleher JJ, Fossette S, Hays GC. Are vertical migrations driven by circadian behaviour? Decoupling of activity and depth use in a large riverine elasmobranch, the freshwater sawfish (Pristis pristis). Hydrobiologia. 2016;787(1):181–91.

63. Whitney NM, Lear KO, Gleiss AC, Payne N, White CF. Advances in the application of high-resolution biologgers to elasmobranch fishes. In: Carrier JC, Heithaus MR, Simpfendorfer CA, editors. Shark Research: Emerging Technologies and Applications for the Field and Laboratory. CRC Marine Biology Series. Boca Raton, FL: CRC Press; 2018. p. 45–69.

64. Whitney NM, White CF, Gleiss AC, Schwieterman GD, Anderson P, Hueter RE, et al. A novel method for determining post-release mortality, behavior, and recovery period using acceleration data loggers. Fisheries Research. 2016;183:210–21.

65. Weihs D. Mechanically efficient swimming techniques for fish with negative buoyancy. Journal of Marine Research. 1973;31:194–209.

66. Papastamatiou YP, Iosilevskii G, Leos-Barajas V, Brooks EJ, Howey LA, Chapman DD, et al. Optimal swimming strategies and behavioral plasticity of oceanic whitetip sharks. Scientific Reports. 2018;8(1):551. doi: 10.1038/s41598-017-18608-z 29323131

67. Grubbs RD, Cotton C, Daly-Engel T, Kerstetterm D. Post-release survival and vertical movements of bluntnose sixgill sharks (Hexanchus griseus) in four oceanic regions. 30th American Elasmobranch Society Symposium; Chattanooga, TN2014.

68. Bingham FM, Lukas R. Seasonal cycles of temperature, salinity and dissolved oxygen observed in the Hawaii Ocean Time-series. Deep Sea Research Part II: Topical Studies in Oceanography. 1996;43(2):199–213.

69. Karl DM, Lukas R. The Hawaii Ocean Time-series (HOT) program: background, rationale and field implementation. Deep Sea Research Part II: Topical Studies in Oceanography. 1996;43(2):129–56.

70. Watanabe YY, Lydersen C, Fisk AT, Kovacs KM. The slowest fish: swim speed and tail-beat frequency of Greenland sharks. Journal of Experimental Marine Biology and Ecology. 2012;426–427:5–11.

71. Jacoby DM, Siriwat P, Freeman R, Carbone C. Is the scaling of swim speed in sharks driven by metabolism? Biology letters. 2015;11(12):20150781. doi: 10.1098/rsbl.2015.0781 26631246

72. Childress JJ. Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends in Ecology & Evolution. 1995;10(1):30–6.

73. Drazen JC, Seibel BA. Depth-related trends in metabolism of benthic and benthopelagic deep-sea fishes. Limnology and Oceanography. 2007;52(5):2306–16.

74. Seibel BA, Drazen JC. The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities. Philosophical Transactions of the Royal Society B: Biological Sciences. 2007;362(1487):2061–78. doi: 10.1098/rstb.2007.2101 17510016

75. Condon NE, Friedman JR, Drazen JC. Metabolic enzyme activities in shallow- and deep-water chondrichthyans: implications for metabolic and locomotor capacity. Marine Biology. 2012;159(8):1713–31.

76. Almeida-Val VM, Val AL, Duncan WP, Souza FC, Paula-Silva MN, Land S. Scaling effects on hypoxia tolerance in the Amazon fish Astronotus ocellatus (Perciformes: Cichlidae): contribution of tissue enzyme levels. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology. 2000;125(2):219–26.

77. Nilsson GE, Östlund‐Nilsson S. Does size matter for hypoxia tolerance in fish? Biological Reviews. 2008;83(2):173–89. doi: 10.1111/j.1469-185X.2008.00038.x 18397180

78. Urbina MA, Glover CN. Relationship between fish size and metabolic rate in the oxyconforming inanga Galaxias maculatus reveals size-dependent strategies to withstand hypoxia. Physiological and Biochemical Zoology. 2013;86(6):740–9. doi: 10.1086/673727 24241070

79. Friedman JR, Condon NE, Drazen JC. Gill surface area and metabolic enzyme activities of demersal fishes associated with the oxygen minimum zone off California. Limnology and Oceanography. 2012;57(6):1701–10.

80. Herbert NA, Skov PV, Tirsgaard B, Bushnell PG, Brill RW, Harvey Clark C, et al. Blood O2 affinity of a large polar elasmobranch, the Greenland shark Somniosus microcephalus. Polar Biology. 2017;40(11):2297–305.

81. Weng KC, Castilho PC, Morrissette JM, Landeira-Fernandez AM, Holts DB, Schallert RJ, et al. Satellite tagging and cardiac physiology reveal niche expansion in salmon sharks. Science. 2005;310(5745):104–6. doi: 10.1126/science.1114616 16210538

82. Madigan DJ, Carlisle AB, Gardner LD, Jayasundara N, Micheli F, Schaefer KM, et al. Assessing niche width of endothermic fish from genes to ecosystem. Proceedings of the National Academy of Sciences. 2015;112(27):8350–5.

83. Watanabe YY, Goldman KJ, Caselle JE, Chapman DD, Papastamatiou YP. Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes. Proceedings of the National Academy of Sciences. 2015;112(19):6104–9.

84. Carey FG, Scharold JV. Movements of blue sharks (Prionace glauca) in depth and course. Marine Biology. 1990;106:329–42.

85. West GJ, Stevens JD. Archival tagging of school shark, Galeorhinus galeus, in Australia—initial results. Environmental Biology of Fishes. 2001;60:283–98.

86. Hulbert LB, Sigler MF, Lunsford CR. Depth and movement behaviour of the Pacific sleeper shark in the north-east Pacific Ocean. Journal of Fish Biology. 2006;69(2):406–25.

87. Stoehr A, St. Martin J, Aalbers S, Sepulveda C, Bernal D, Eliason EJ. Free-swimming swordfish, Xiphias gladius, alter the rate of whole body heat transfer: morphological and physiological specializations for thermoregulation. ICES Journal of Marine Science. 2018;75(2):858–70.

88. Hight BV, Lowe CG. Elevated body temperatures of adult female leopard sharks, Triakis semifasciata, while aggregating in shallow nearshore embayments: evidence for behavioral thermoregulation? Journal of Experimental Marine Biology and Ecology. 2007;352(1):114–28.

89. Meekan MG, Fuiman LA, Davis R, Berger Y, Thums M. Swimming strategy and body plan of the world's largest fish: implications for foraging efficiency and thermoregulation. Frontiers in Marine Science. 2015;2:64.

90. Langrock R, Kneib T, Sohn A, DeRuiter SL. Nonparametric inference in hidden Markov models using P-splines. Biometrics. 2015;71(2):520–8. doi: 10.1111/biom.12282 25586063

91. Crow GL, Lowe CG, Wetherbee BM. Shark records from longline fishing programs in Hawai'i with comments on Pacific Ocean distributions. Pacific Science. 1996;50(4):382–92.

92. Meyer CG, Holland KN. Autonomous measurement of ingestion and digestion processes in free-swimming sharks. Journal of Experimental Biology. 2012;215(21):3681–4.

93. Papastamatiou YP, Meyer CG, Watanabe YY, Heithaus MR. Animal-borne video cameras and their use to study shark ecology and conservation. In: Carrier JC, Heithaus MR, Simpfendorfer CA, editors. Shark Research: Emerging Technologies and Applications for the Field and Laboratory. CRC Marine Biology Series. Boca Raton, FL: CRC Press; 2018. p. 83–92.

Diel patterns in swimming behavior of a vertically migrating deepwater shark, the bluntnose sixgill (Hexanchus griseus)

Souhrn

Klíčová slova:

Zdroje

PLOS One

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií

Aktuální možnosti diagnostiky a léčby litiáz