Behavioural responses to hydrostatic pressure in selected echinoderms suggest hyperbaric constraint of bathymetric range
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.
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.
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Conflict of interest
The authors declare that they have no conflict of interest
All necessary international, national and institutional protocols for the care and use of animals were followed.
- 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
- Cavey MJ, Märkel K (1994) Echinoidea. In: Harrison FW, China FS (eds) Microscopic anatomy of invertebrates, Echinodermata. Wiley-Liss Inc, New York, pp 345–400Google Scholar
- 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):357–363CrossRefPubMedGoogle Scholar
- 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)Google Scholar
- 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):333–336Google Scholar
- Doyle WL, McNiell GF (1964) The fine structure of the respiratory tree in Cucumaria. Q J Microsc Sci 3(69):7–11Google Scholar
- 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):915–922Google Scholar
- 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 79–93Google Scholar
- Hochachka P, Somero G (1984) Temperature adaptation. Biochemical adaptation. Princeton University Press, Princeton, pp 355–449Google Scholar
- Lawrence JM (1987) Functional biology of echinoderms. Croom Helm, LondonGoogle Scholar
- 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 181:9–17CrossRefPubMedGoogle Scholar
- 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):150472CrossRefPubMedPubMedCentralGoogle Scholar
- Pradillion F (2011) High hydrostatic pressure environments. In: Bell E (ed) Life at extremes: environments, organisms, and strategies for survival. CABI, Wallingford, pp 271–295Google Scholar
- 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
- Stasek CR (1967) Autotomy in the mollusca. Occas Pap Calif Acad Sci 61:1–44Google Scholar
- Thistle D (2003) The deep-sea floor: an overview. In: Tyler PA (ed) Ecosystems of the World. Elsevier, Amsterdam, pp 5–38Google Scholar
- WoRMS Editorial Board (2014) World register of marine species. http://www.marinespecies.org. Accessed 09 Aug 2014