Abstract
Although hydrostatic pressure is one of the most prominent abiotic drivers of faunal bathymetric ranges, it is one of the least understood. To better understand hyperbaric constraints on depth distributions, we explored responses to high pressure of adult echinoderms from eastern Canada. The sea urchin Strongylocentrotus droebachiensis, the sea star Leptasterias polaris and the sea cucumber Cucumaria frondosa were exposed to various pressures within and beyond their known bathymetric distribution (i.e. surface pressure; pressure at the midpoint in bathymetric distribution; pressure at twice the maximum depth in the species bathymetric distribution) for different durations (24 h, 72 h, 9 days). Survival was compromised by exposure to the highest pressure levels, with the sea urchin exhibiting the highest mortality. After 72-h exposure, mortality was observed for sea urchin and sea cucumber individuals while all sea star individuals survived. Following 9-day exposure of sea star individuals to high pressure, 100% mortality occurred. Exposure to pressures typical of natural distributions had little effect on the selected health and motor metrics. Pressures atypical of natural ranges negatively affected the motor functions of all species, irrespective of exposure duration. During and after 24-h exposure, feeding was reduced in sea urchin and sea cucumber individuals, but was unchanged in sea star individuals. Overall, there were no clear signs of acclimation to high pressure following sustained periods of exposure in any species. These results highlight constraints applied by hydrostatic pressure beyond current bathymetric ranges on life-sustaining behaviours in echinoderms. The potential of long-lived echinoderms to survive downward migration to greater depths is species-specific, suggesting there may be winners and losers in the face of near-future climate-driven migration patterns.
Similar content being viewed by others
References
Abe T, Kakyo M, Tokui T, Nakagomi R, Nishio T, Nakai D, Nomura H, Unno M, Suzuki M, Naitoh T, Matsuno S, Yawo H (1999) Identification of a novel gene family encoding human liver-specific organic anion transporter LST-1. J Biol Chem 274(24):17159–17163
Amaro T, Witte H, Herndl GJ, Cunha MR, Billett DS (2009) Deep-sea bacterial communities in sediments and guts of deposit-feeding holothurians in Portuguese canyons (NE Atlantic). Deep Sea Res I 56(10):1834–1843
Appelhans YS, Thomsen J, Opitz S, Pansch C, Melzner F, Wahl M (2014) Juvenile sea stars exposed to acidification decrease feeding and growth with no acclimation potential. Mar Ecol Prog Ser 509:227–239
Aquino-Souza R, Hawkins S, Tyler P (2008) Early development and larval survival of Psammechinus miliaris under deep-sea temperature and pressure conditions. J Mar Biol Assoc UK 88(3):453–461
Balny C, Mozhaev VV, Lange R (1997) Hydrostatic pressure and proteins: basic concepts and new data. Comp Biochem Physiol A Physiol 116(4):299–304
Bett BJ, Malzone MG, Narayanaswamy BE, Wigham BD (2001) Temporal variability in phytodetritus and megabenthic activity at the seabed in the deep northeast Atlantic. Prog Oceanogr 50(1):349–368
Bowser-Riley F (1984) Mechanistic studies on the high pressure neurological syndrome. Philos Trans R Soc Lond B Biol Sci 304(1118):31–41
Brierley AS, Kingsford MJ (2009) Impacts of climate change on marine organisms and ecosystems. Curr Biol 19(14):602–614
Brodie B, Mowbray F, Power D (2013) DFO Newfoundland and Labrador region ecosystem trawl surveys. OBIS Canada digital collections. Bedford Institute of Oceanography, Dartmouth, NS, Canada. http://www.iobis.org/. Accessed 09 Aug 2014
Brooke SD, Young CM (2009) Where do the embryos of Riftia pachyptila develop? Pressure tolerances, temperature tolerances, and buoyancy during prolonged embryonic dispersal. Deep Sea Res II 56(19):1599–1606
Brown A, Thatje S (2014) Explaining bathymetric diversity patterns in marine benthic invertebrates and demersal fishes: physiological contributions to adaptation of life at depth. Biol Rev 89(2):406–426
Brown A, Thatje S (2015) The effects of changing climate on faunal depth distributions determine winners and losers. Glob Change Biol 21(1):173–180
Brown A, Thatje S (2018) NMDA receptor regulation is involved in the limitation of physiological tolerance to both low temperature and high hydrostatic pressure. Front Mar Sci 5:93
Brown A, Thatje S, Morris JP, Oliphant A, Morgan EA, Hauton C, Jones DO, Pond DW (2017) Metabolic costs imposed by hydrostatic pressure constrain bathymetric range in the lithodid crab Lithodes maja. J Exp Biol 220(21):3916–3926
Brown A, Hauton C, Stratmann T, Sweetman A, van Oevelen D, Jones DO (2018) Metabolic rates are significantly lower in abyssal holothuroidea than in shallow-water holothuroidea. R Soc Open Sci 5(5):172162
Carney RS (2005) Zonation of deep biota on continental margins. Oceanogr Mar Biol 43:211–227
Cavey MJ, Märkel K (1994) Echinoidea. In: Harrison FW, China FS (eds) Microscopic anatomy of invertebrates, Echinodermata. Wiley-Liss Inc, New York, pp 345–400
Childress JJ (1995) Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends Ecol Evol 10(1):30–36
Company J, Sardà F (1998) Metabolic rates and energy content of deep-sea benthic decapod crustaceans in the western Mediterranean Sea. Deep Sea Res I 45(11):1861–1880
Cottin D, Brown A, Oliphant A, Mestre NC, Ravaux J, Shillito B, Thatje S (2012) Sustained hydrostatic pressure tolerance of the shallow water shrimp Palaemonetes varians at different temperatures: insights into the colonisation of the deep sea. Comp Biochem Physiol A Mol Integr Physiol 162(4):357–363
DFO (2009) State of the ocean: physical oceanographic conditions in the Newfoundland and Labrador region DFO (Canadian Science Advisory Secretariat Science Advisory Report 2009/057)
Ding J, Chang Y, Wang Z, Song J (2007) Polyploidy induction by hydrostatic pressure shock and embryo development of sea cucumber Apostichopus japonicus. Chin J Oceanol Limnol 25:184–190
Dixon DR, Dixon LR, Shillito B, Gwynn JP (2002) Background and induced levels of DNA damage in Pacific deep-sea vent polychaetes: the case for avoidance. Cah Biol Mar 43(3/4):333–336
Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N (2012) Climate change impacts on marine ecosystems. Mar Sci 4:11–37
Doyle WL, McNiell GF (1964) The fine structure of the respiratory tree in Cucumaria. Q J Microsc Sci 3(69):7–11
Ebert TA, Southon JR (2003) Red sea urchins (Strongylocentrotus franciscanus) can live over 100 years: confirmation with A-bomb 14carbon. Fish Bull NOAA 101(4):915–922
Ellers O, Telford M (1992) Causes and consequences of fluctuating coelomic pressure in sea urchins. Biol Bull 182(3):424–434
Feder HM (1963) Gastropod defensive responses and their effectiveness in reducing predation by starfishes. Ecology 44(3):505–512
Feder HM (1972) Escape responses in marine invertebrates. Sci Am 227:92–100
Ferguson JC (1992) The function of the madreporite in body fluid volume maintenance by an intertidal starfish, Pisaster ochraceus. Biol Bull 183(3):482–489
Gage JD, Tyler PA (1991) Deep-sea biology: a natural history of organisms at the deep-sea floor. Cambridge University Press, Cambridge
Gardiner SL, Rieger RM (1980) Rudimentary cilia in muscle cells of annelids and echinoderms. Cell Tissue Res 213(2):247–252
Gianasi BL, Verkaik K, Hamel J-F, Mercier A (2015) Novel use of PIT tags in sea cucumbers: promising results with the commercial species Cucumaria frondosa. PLoS One 10(5):e0127884
Graham MH, Kinlan BP, Druehl LD, Garske LE, Banks S (2007) Deep-water kelp refugia as potential hotspots of tropical marine diversity and productivity. Proc Natl Acad Sci 104(42):16576–16580
Harley CD, Randall Hughes A, Hultgren KM, Miner BG, Sorte CJ, Thornber CS, Rodriguez LF, Tomanek L, Williams SL (2006) The impacts of climate change in coastal marine systems. Ecol Lett 9(2):228–241
Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29(3):167–227
Hessler RR (1974) The structure of deep benthic communities from central oceanic waters. In: Miller CM (ed) The biology of the oceanic Pacific. Oregon State University Press, Princeton, pp 79–93
Hochachka P, Somero G (1984) Temperature adaptation. Biochemical adaptation. Princeton University Press, Princeton, pp 355–449
Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world’s marine ecosystems. Science 328(5985):1523–1528
Lawrence JM (1987) Functional biology of echinoderms. Croom Helm, London
LeClair EE (1993) Effects of anatomy and environment on the relative preservability of asteroids: a biomechanical comparison. Palaios 8:233–243
Macdonald AG (1972) The role of high hydrostatic pressure in the physiology of marine animals. Symp Soc Exp Biol 26:209–231
Macdonald AG (1984) The effects of pressure on the molecular structure and physiological functions of cell membranes. Philos Trans R Soc Lond B Biol Sci 304(1118):47–68
Macdonald A (1997) Hydrostatic pressure as an environmental factor in life processes. Comp Biochem Physiol A Physiol 116(4):291–297
Macdonald A, Gilchrist I (1978) Further studies on the pressure tolerance of deep-sea crustacea, with observations using a new high-pressure trap. Mar Biol 45(1):9–21
MacDonald IR, Bluhm BA, Iken K, Gagaev S, Strong S (2010) Benthic macrofauna and megafauna assemblages in the arctic deep-sea Canada basin. Deep Sea Res II 57(1):136–152
Meidel S, Scheibling RE (1999) Effects of food type and ration on reproductive maturation and growth of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 134(1):155–166
Mickel TJ, Childress J (1982a) Effects of pressure and pressure acclimation on activity and oxygen consumption in the bathypelagic mysid Gnathophausia ingens. Deep Sea Res Part A 29(11):1293–1301
Mickel TJ, Childress JJ (1982b) Effects of pressure and temperature on the EKG and heart rate of the hydrothermal vent crab Bythograea thermydron (Brachyura). Biol Bull 162(1):70–82
Miyake H, Kitada M, Tsuchida S, Okuyama Y, Nakamura K (2007) Ecological aspects of hydrothermal vent animals in captivity at atmospheric pressure. Mar Ecol 28(1):86–92
Miyake H, Lindsay DJ, Kitada M, Nemoto S, Miwa T, Itoh T (2012) How to keep deep-sea animals. INTECH Open Access Publisher, Tokyo
Morris J, Thatje S, Ravaux J, Shillito B, Fernando D, Hauton C (2015a) Acute combined pressure and temperature exposures on a shallow-water crustacean: novel insights into the stress response and high pressure neurological syndrome. Comp Biochem Physiol A Mol Integr Physiol 181:9–17
Morris J, Thatje S, Cottin D, Oliphant A, Brown A, Shillito B, Ravaux J, Hauton C (2015b) The potential for climate-driven bathymetric range shifts: sustained temperature and pressure exposures on a marine ectotherm, Palaemonetes varians. R Soc Open Sci 2(11):150472
Morris JP, Thatje S, Ravaux J, Shillito B, Hauton C (2015c) Characterising multi-level effects of acute pressure exposure on a shallow-water invertebrate: insights into the kinetics and hierarchy of the stress response. J Exp Biol 218(16):2594–2602
New P, Brown A, Oliphant A, Burchell P, Smith A, Thatje S (2014) The effects of temperature and pressure acclimation on the temperature and pressure tolerance of the shallow-water shrimp Palaemonetes varians. Mar Biol 161(3):697–709
Oliphant A, Thatje S, Brown A, Morini M, Ravaux J, Shillito B (2011) Pressure tolerance of the shallow-water caridean shrimp Palaemonetes varians across its thermal tolerance window. J Exp Biol 214(7):1109–1117
Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308(5730):1912–1915
Pond DW, Tarling GA, Mayor DJ (2014) Hydrostatic pressure and temperature effects on the membranes of a seasonally migrating marine copepod. PLoS One 9(10):e111043
Pradillion F (2011) High hydrostatic pressure environments. In: Bell E (ed) Life at extremes: environments, organisms, and strategies for survival. CABI, Wallingford, pp 271–295
Pradillon F, Gaill F (2007) Pressure and life: some biological strategies. Rev Environ Sci Biotechnol 6(1–3):181–195
Pradillon F, Shillito B, Chervin J, Hamel G, Gaill F (2004) Pressure vessels for in vivo studies of deep-sea fauna. High Press Res 24(2):237–246
Ramsay K, Turner JR, Vize SJ, Richardson CA (2000) A link between predator density and arm loss in the starfish Marthasterias glacialis and Asterias rubens. J Mar Biol Assoc UK 80(3):565–566
Ramsay K, Bergmann M, Veale L, Richardson C, Kaiser M, Vize S, Feist S (2001) Damage, autotomy and arm regeneration in starfish caught by towed demersal fishing gears. Mar Biol 138(3):527–536
Ravaux J, Gaill F, Le Bris N, Sarradin PM, Jollivet D, Shillito B (2003) Heat-shock response and temperature resistance in the deep-sea vent shrimp Rimicaris exoculata. J Exp Biol 206(14):2345–2354
Ravaux J, Cottin D, Chertemps T, Hamel G, Shillito B (2009) Hydrothermal shrimps display low expression of heat-inducible hsp70 gene in nature. Mar Ecol Prog Ser 396:153–156
Robinson NJ, Thatje S, Osseforth C (2009) Heartbeat sensors under pressure: a new method for assessing hyperbaric physiology. High Press Res 29(3):422–430
Rochette R, Hamel J-F, Himmelman JH (1994) Foraging strategy of the asteroid Leptasterias polaris: role of prey odors, current and feeding status. Mar Ecol Prog Ser 106:93
Ross DA, Hamel J-F, Mercier A (2013) Bathymetric and interspecific variability in maternal reproductive investment and diet of eurybathic echinoderms. Deep Sea Res II 94:333–342
Schlieper C (1968) High pressure effects on marine invertebrates and fishes. Mar Biol 2(1):5–12
Shillito B, Jollivet D, Sarradin P, Rodier P, Lallier F, Desbruyères D, Gaill F (2001) Temperature resistance of Hesiolyra bergi, a polychaetous annelid living on deep-sea vent smoker walls. Mar Ecol Prog Ser 216:141–149
Shillito B, Bris NL, Gaill F, Rees J, Zal F (2004) First access to live alvinellas. High Press Res 24(1):169–172
Shillito B, Le Bris N, Hourdez S, Ravaux J, Cottin D, Caprais JC, Jollivet D, Gaill F (2006) Temperature resistance studies on the deep-sea vent shrimp Mirocaris fortunata. J Exp Biol 209(5):945–955
Shillito B, Ravaux J, Sarrazin J, Zbinden M, Sarradin P, Barthelemy D (2015) Long-term maintenance and public exhibition of deep-sea hydrothermal fauna: the AbyssBox project. Deep Sea Res II 121:137–145
Smithsonian Institution (1974) Department of Invertebrate Zoology, Research and Collections Information System, NMNH, Smithsonian Institution. http://www.mnh.si.edu/rc/db/collection_db_policy1.html. Accessed 09 Aug 2014
So J, Hamel J-F, Mercier A (2010) Habitat utilisation, growth and predation of Cucumaria frondosa: implications for an emerging sea cucumber fishery. Fish Manag Ecol 17(6):473–484
Sokolova IM (2013) Energy-limited tolerance to stress as a conceptual framework to integrate the effects of multiple stressors. Integr Comp Biol 53(4):597–608
Somero G (1992) Biochemical ecology of deep-sea animals. Experientia 48(6):537–543
Stasek CR (1967) Autotomy in the mollusca. Occas Pap Calif Acad Sci 61:1–44
Swezey RR, Somero GN (1985) Pressure effects on actin self-assembly: interspecific differences in the equilibrium and kinetics of the G to F transformation. Biochemistry 24(4):852–860
Takahashi K, Kubo T, Arai Y, Kitajima I, Takigawa M, Imanishi J, Hirasawa Y (1998) Hydrostatic pressure induces expression of interleukin 6 and tumour necrosis factor alpha mRNAs in a chondrocyte-like cell line. Ann Rheum Dis 57(4):231–236
Taylor J, Lovera C, Whaling P, Buck K, Pane E, Barry J (2014) Physiological effects of environmental acidification in the deep-sea urchin Strongylocentrotus fragilis. Biogeosciences 11(5):1413–1423
Thatje S, Robinson N (2011) Specific dynamic action affects the hydrostatic pressure tolerance of the shallow-water spider crab Maja brachydactyla. Naturwissenschaften 98(4):299–313
Thatje S, Casburn L, Calcagno JA (2010) Behavioural and respiratory response of the shallow-water hermit crab Pagurus cuanensis to hydrostatic pressure and temperature. J Exp Mar Biol Ecol 390(1):22–30
Thistle D (2003) The deep-sea floor: an overview. In: Tyler PA (ed) Ecosystems of the World. Elsevier, Amsterdam, pp 5–38
Tyler P, Dixon D (2000) Temperature/pressure tolerance of the first larval stage of Mirocaris fortunata from lucky strike hydrothermal vent field. J Mar Biol Assoc UK 80(4):739–740
Tyler P, Young C (1998) Temperature and pressure tolerances in dispersal stages of the genus Echinus (Echinodermata: Echinoidea): prerequisites for deep-sea invasion and speciation. Deep Sea Res II 45(1):253–277
Tyler PA, Young CM, Clarke A (2000) Temperature and pressure tolerances of embryos and larvae of the antarctic sea urchin Sterechinus neumayeri (Echinodermata: Echinoidea): potential for deep-sea invasion from high latitudes. Mar Ecol Prog Ser 192:173–180
VandenSpiegel D, Jangoux M (1987) Cuvierian tubules of the holothuroid Holothuria forskali (Echinodermata): a morphofunctional study. Mar Biol 96(2):263–275
Verkaik K, Hamel J-F, Mercier A (2016) Carry-over effects of ocean acidification in a cold-water lecithotrophic holothuroid. Mar Ecol Prog Ser 557:189–206
Villalobos FB, Tyler PA, Young CM (2006) Temperature and pressure tolerance of embryos and larvae of the Atlantic seastars Asterias rubens and Marthasterias glacialis (Echinodermata: Asteroidea): potential for deep-sea invasion. Mar Ecol Prog Ser 314:109–117
Wessel GM, Fresques T, Kiyomoto M, Yajima M, Zazueta V (2014) Origin and development of the germ line in sea stars. Genesis 52(5):367–377
Wilcock S, Wann K, Macdonald A (1978) The motor activity of Crangon crangon subjected to high hydrostatic pressure. Mar Biol 45(1):1–7
WoRMS Editorial Board (2014) World register of marine species. http://www.marinespecies.org. Accessed 09 Aug 2014
Yoshiki T, Yamanoha B, Kikuchi T, Shimizu A, Toda T (2008) Hydrostatic pressure-induced apoptosis on nauplii of Calanus sinicus. Mar Biol 156(2):97–106
Young CM, Tyler PA (1993) Embryos of the deep-sea echinoid Echinus affinis require high pressure for development. Limnol Oceanogr 38(1):178–181
Young CM, Vázquez E, Metaxas A, Tyler PA (1996) Embryology of vestimentiferan tube worms from deep-sea methane/sulphide seeps. Nature 381(6582):514–516
Young C, Tyler P, Fenaux L (1997) Potential for deep sea invasion by Mediterranean shallow water echinoids: pressure and temperature as stage-specific dispersal barriers. Mar Ecol Prog Ser 154:197–209
Acknowledgements
We would like to thank the Ocean Sciences Centre Field Services (Memorial University) for the animal collections and the two reviewers for helpful comments on the manuscript. We also extend our thanks to Gordon Nash and Stephen Hills for technical help with the IPOCAMP systems, as well as to Camilla Parzanini, Emy Montgomery, and Matt Osse for their invaluable support. This research was supported by Grants from the Natural Science and Engineering Research Council (NSERC), the Canadian Foundation for Innovation (CFI) and the Research and Development Corporation (RDC) of Newfoundland and Labrador to Annie Mercier.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest
Ethical standards
All necessary international, national and institutional protocols for the care and use of animals were followed.
Additional information
Responsible Editor: M. Byrne.
Reviewed by C. Young and an undisclosed expert.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ammendolia, J., Hamel, JF. & Mercier, A. Behavioural responses to hydrostatic pressure in selected echinoderms suggest hyperbaric constraint of bathymetric range. Mar Biol 165, 145 (2018). https://doi.org/10.1007/s00227-018-3399-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-018-3399-7