Skip to main content
Log in

Temperature and salinity tolerances of embryos and larvae of the deep-sea mytilid mussel “Bathymodioluschildressi

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

We examined temperature and salinity tolerances of early embryonic and larval stages of the deep-sea, cold-seep mussel “Bathymodiolus” childressi to determine whether they may control the dispersal depth of larvae. Salinity and temperature tolerances increased with developmental stage, but tolerance ranges were not as wide for the larvae of “B.” childressi as for the larvae of the related shallow-water mussel Mytilus trossulus. Normal development occurred in “B.” childressi from 7 to 15°C and at salinities of 35 and 45. Greater tolerance of “B.” childressi embryos to high than low salinities may aid development of negatively buoyant early embryos at brine seeps. Although there was a decreasing trend in survival of “B.” childressi larvae with increasing temperature, survival of “B.” childressi trochophores was not significantly different at 20°C than at the adults’ ambient temperature. Since larvae tolerate increasing temperatures as they age and seawater temperatures at 100 m depth do not exceed 20°C in months following the mussels’ spawning season, we suggest that temperature would not limit vertical migration of the veliger larvae of “B.” childressi into even the uppermost layer of the water column above the cold seeps in the Gulf of Mexico.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Notes

  1. We place the genus name of “Bathymodiolus” childressi in quotation marks following nomenclature recommendations due to taxonomic uncertainty raised by both morphology (Gustafson et al. 1998) and molecular phylogeny (Jones et al. 2006).

References

  • Arellano SM (2008) Embryology, larval ecology, and recruitment of “Bathymodiolus” childressi, a cold seep mussel from the Gulf of Mexico. Dissertation, University of Oregon

  • Arellano SM, Young CM (2009) Spawning, development, and the duration of larval life in a deep-sea cold-seep mussel. Biol Bull 216:149–162

    Article  Google Scholar 

  • Arellano SM, Young CM (2010) Pre- and post-settlement factors controlling spatial variation in recruitment across a cold-seep mussel bed. Mar Ecol Prog Ser 414:131–144

    Article  Google Scholar 

  • Bartholomew GA (1987) Interspecific comparison as a tool for ecological physiologists. In: Feder ME, Bennett AF, Burgren WW, Huey RB (eds) New directions in ecological physiology. Cambridge University Press, Cambridge, pp 11–37

    Google Scholar 

  • Bayne BL (1965) Growth and the delay of metamorphosis of the larvae of Mytilus edulis (L.). Ophelia 2(1):1–47

    Article  Google Scholar 

  • Bayne BL (1972) Some effects of stress in the adult on the larval development of Mytilus edulis. Nature 237:459

    Article  CAS  Google Scholar 

  • Bayne BL (1976) The biology of mussel larvae. In: Bayne BL (ed) Marine mussels: their ecology and physiology. Cambridge University Press, Cambridge, pp 81–120

    Google Scholar 

  • Bayne BL, Gabbott PA, Widdows J (1975) Some effects of stress in the adult on the eggs and larvae of Mytilus edulis L. J Mar Biol Assoc UK 55:675–689

    Article  Google Scholar 

  • Bayne BL, Holland DL, Moore MN, Lowe DM, Widdows J (1978) Further studies on the effects of stress in the adult on the eggs of Mytilus edulis. J Mar Biol Assoc UK 58:825–841

    Article  Google Scholar 

  • Berger MS, Young CM (2006) Physiological response of the cold-seep mussel Bathymodiolus childressi to acutely elevated temperature. Mar Biol 149:1397–1402

    Article  Google Scholar 

  • Bouchet P, Warén A (1994) Ontogenetic migration and dispersal of deep-sea gastropod larvae. In: Young CM, Eckelbarger KJ (eds) Reproduction, larval biology, and recruitment of the deep-sea benthos. Columbia University Press, New York, pp 98–119

    Google Scholar 

  • Braby CE, Somero GN (2006a) Ecological gradients and relative abundance of native (Mytilus trossulus) and invasive (Mytilus galloprovincialis) blue mussels in the California hyrbrid zone. Mar Biol 148:1249–1262

    Article  Google Scholar 

  • Braby CE, Somero GN (2006b) Following the heart: temperature and salinity effects on heart rate in native and invasive species of blue mussels (genus Mytilus). J Exp Biol 209:2554–2566

    Article  Google Scholar 

  • 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 56:1599–1606

    Article  Google Scholar 

  • Carney SL, Formica MI, Divatia H, Nelson K, Fisher CR, Schaeffer SW (2006) Population structure of the mussel “Bathymodiolus” childressi from Gulf of Mexico hydrocarbon seeps. Deep-Sea Res I 53(6):1061–1072

    Article  Google Scholar 

  • Charmantier G, Wolcott DL (2001) Introduction to the symposium: ontogenetic strategies of invertebrates in aquatic environments. Am Zool 41:1053–1056

    Google Scholar 

  • Chia F, Buckland-Nicks SJ, Young CM (1984) Locomotion of marine invertebrate larvae: a review. Can J Zool 62:1205–1222

    Article  Google Scholar 

  • Childress JJ, Fisher CR, Brooks JM, Kennicutt MC II, Bidigare RR, Anderson AE (1986) A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: mussels fueled by gas. Science 233:1306–1308

    Article  CAS  Google Scholar 

  • Clarke A (1983) Life in cold water: the physiological ecology of polar marine ectotherms. Oceanogr Mar Biol Annu Rev 21:341–453

    Google Scholar 

  • Craddock C, Hoeh WR, Gustafson RG, Lutz RA, Hashimoto J, Vrijenhoek RC (1995) Evolutionary relationships among deep-sea mytilids (Bivalvia: Mytilidae) from hydrothermal vents and cold-water methane/sulfide seeps. Mar Biol 121:477–485

    Article  Google Scholar 

  • Distel DL (2000) Phylogenetic relationships among Mytilidae (Bivalvia): 18S rRNA data suggest convergence in mytilid body plans. Mol Phylogen Evol 15:25–33

    Article  CAS  Google Scholar 

  • Eckelbarger KJ, Watling L (1995) Role of phylogenetic constraints in determining reproductive patterns in deep-sea invertebrates. Invertebr Biol 114(3):256–269

    Article  Google Scholar 

  • Gosling EM (2003) Bivalve molluscs: biology, ecology and culture. Oxford Press, Malden

    Book  Google Scholar 

  • Gustafson RG, Lutz RA (1994) Molluscan life history traits at deep-sea hydrothermal vents and cold methane/sulfide seeps. In: Young CM, Eckelbarger KJ (eds) Reproduction, larval biology, and recruitment of the deep-sea benthos. Columbia University Press, Columbia, pp 76–97

    Google Scholar 

  • Gustafson RG, Turner RD, Lutz RA, Vrijenhoek RC (1998) A new genus and five species of mussels (Bivalvia, Mytilidae) from deep-sea sulfide/hydrocarbon seeps in the Gulf of Mexico. Malacologia 40(1–2):63–112

    Google Scholar 

  • Hayhurst S, Rawson PD (2009) Species specific variation in larval survival and patterns of distribution for the blue mussels Mytilus edulis and Mytilus trossulus in the Gulf of Maine. J Moll Stud 75:215–222

    Article  Google Scholar 

  • His E, Robert R, Dinet A (1984) Combined effects of temperature and salinity on fed and starved larvae of the Mediterranean mussel Mytilus galloprovincialis and the Japanese oyster Crassostrea gigas. Mar Biol 100:455–463

    Article  Google Scholar 

  • Hrs-Brenko M, Calabrese A (1969) The combined effects of salinity and temperature on larvae of the mussel Mytilus edulis. Mar Biol 4(3):224–226

    Article  Google Scholar 

  • Jones WJ, Won Y-J, Maas PAY, Smith PJ, Lutz RA, Vrijenhoek RC (2006) Evolution of habitat use by deep-sea mussels. Mar Biol 148:841–851

    Article  Google Scholar 

  • Kinne O (1970) Temperature-invertebrates. In: Kinne O (ed) Marine ecology vol I Part 1. Wiley-Interscience, London, pp 405–514

    Google Scholar 

  • Kinne O (1971) Salinity-invertebrates. In: Kinne O (ed) Marine ecology vol. I Part 2. Wiley-Interscience, London, pp 821–874

    Google Scholar 

  • Li Y, Nowlin D Jr, Reid RO (1997) Mean hydrographic fields and their interannual variability over the Texas Louisiana continental shelf in spring, summer, and fall. J Geophys Res 102:1027–1049

    Article  Google Scholar 

  • Limbeck SJ (2003) The role of larval thermal tolerance in the distribution of blue mussel species within the Gulf o f Maine. MS Thesis, University of Maine

  • Lutz RA, Jablonski D, Rhoads DC, Turner RD (1980) Larval dispersal of a deep-sea hydrothermal vent bivalve from the Galapagos Rift. Mar Biol 57:127–133

    Article  Google Scholar 

  • Lutz RA, Jablonski D, Turner RD (1984) Larval dispersal at deep-sea hydrothermal vents. Science 226:1451–1454

    Article  CAS  Google Scholar 

  • MacDonald IR (1998) Stability and change in Gulf of Mexico chemosynthetic communities: Interim report. Prepared for the Department of the Interior, Minerals Management Service, Gulf of Mexico OCS Region, p 409

    Google Scholar 

  • Marsh AG, Mullineaux LS, Young CM, Manahan DT (2001) Larval dispersal potential of the tubeworm Riftia pachyptila at deep-sea hydrothermal vents. Nature 411:77–80

    Article  CAS  Google Scholar 

  • Mestre N, Thatje S, Tyler PA (2009) The ocean is not deep enough: pressure tolerances during early ontogeny of the blue mussel Mytilus edulis. Proc R Soc B 276:717–726

    Article  Google Scholar 

  • Miyake H, Tsukahara J, Hashimoto J, Uematsu K, Maruyama T (2006) Rearing and observation methods of vestimentiferan tubeworm and its early development at atmospheric pressure. Cah Biol Mar 47:471–475

    Google Scholar 

  • Müller-Karger FE, Walsh JJ, Evans RH, Meyers MB (1991) On the seasonal phytoplankton concentration and sea surface temperature cycles of the Gulf of Mexico as determined by satellites. J Geophys Res 96:12645–12665

    Article  Google Scholar 

  • Nix ER, Fisher CR, Vodenichar J, Scott KM (1995) Physiological ecology of a seep mussel with methanotrophic endosymbionts at three hydrocarbon seep sites in the Gulf of Mexico. Mar Biol 122:605–617

    Article  CAS  Google Scholar 

  • O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP, Weiss JM (2007) Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proc Nat Acad Sci 104:1266–1271

    Article  Google Scholar 

  • Pechenik JA (2006) Larval experience and latent effects–metamorphosis is not a new beginning. Integr Comp Biol 46(3):323–333

    Article  Google Scholar 

  • Peck LS, Powell DK, Tyler PA (2007) Very slow development in two Antarctic bivalves molluscs, the infaunal clam Laternula ellicptica and the scallop Adumussium colbecki. Mar Biol 150:1191–1197

    Article  Google Scholar 

  • Pradillon F, Shillito B, Young CM, Gaill F (2001) Developmental arrest in vent worm embryos. Nature 413:698–699

    Article  CAS  Google Scholar 

  • Pradillon F, Le Bris N, Shillito B, Young CM, Gaill F (2005) Influence of environmental conditions on early development of the hydrothermal vent polychaete Alvinella pompejana. J Exp Biol 208:1551–1561

    Article  Google Scholar 

  • Pradillon F, Kawato M, Kubokawa K, Fujiwara Y (2009) Contrasted reproductive and dispersal strategies in Osedax species from different depths around Japan. 4th International Symposium on Chemosynthesis-based Ecosystems. Okinawa, Japan, p 45

    Google Scholar 

  • Qiu JW, Tremblay R, Bourget E (2002) Ontogenetic changes in hyposaline tolerance in the mussels Mytilus edulis and M. trossulus: implications for distribution. Mar Ecol Prog Ser 228:143–152

    Article  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Sameoto JA, Metaxas A (2008) Can salinity-induced mortality explain larval vertical distribution with respect to a halocline? Biol Bull 214:329–338

    Article  Google Scholar 

  • Saranchova OL, Flyachinskaya LP (2001) The influence of salinity on early ontogeny of the mussels Mytilus edulis and the starfish Asteria rubens from the White Sea. Russ J Mar Biol 27(2):87–93

    Article  Google Scholar 

  • Smith EB, Scott KM, Nix ER, Korte C, Fisher CR (2000) Growth and condition of seep mussels (Bathymodiolus childressi) at a Gulf of Mexico brine pool. Ecology 81(9):2392–2403

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. W.H, Freeman and Company, New York

    Google Scholar 

  • Sprung M (1984) Physiological energetics of mussel larvae (Mytilus edulis). I. Shell growth and biomass. Mar Ecol Prog Ser 17:283–293

    Article  Google Scholar 

  • Strathmann MF (1987) Reproduction and development of marine invertebrates of the northern pacific coast: data and methods for the study of eggs, embryos, and larvae. University of Washington Press, Seattle

    Google Scholar 

  • Tyler PA, Young CM, Dolan E, Arellano SM, Brooke SD, Baker M (2006) Gametogenic periodicity in the chemosynthetic cold-seep mussel “Bathymodiolus” childressi. Mar Biol 150(5):829–840

    Article  Google Scholar 

  • UNESCO (United Nations Educational, Scientific and Cultural Organization) (1985) The International System of Units (SI) in Oceanography. Report of IAPSO working group on symbols, units and nomenclature in physical oceanography (SUN). IAPSO Publication Scientifique, no. 32, UNESCO technical papers in marine science, no. 45

  • Van Gaest AL (2006) Ecology and early life history of Bathynerita naticodea: evidence for long-distance larval dispersal of a cold seep gastropod. MS thesis, University of Oregon

  • Yaroslavtseva LM, Sergeeva EP (2006) Adaptivity of the bivalve Mytilus trossulus larvae to short- and long-term changes in water temperature and salinity. Russ J Mar Biol 32(2):82–87

    Article  Google Scholar 

  • Young CM, Tyler PA (1993) Embryos of the deep-sea echinoid Echinus affinis require high pressure for development. Limnol Oceanogr 38:178–181

    Article  Google Scholar 

  • Young CM, Devin MG, Jaeckle WB, Ekaratne SUK, George SB (1996a) The potential for ontogenetic vertical migration by larvae of bathyal echinoderms. Oceanol Acta 19:263–271

    Google Scholar 

  • Young CM, Gage JD, Tyler PA (1996b) Vertical distribution correlates with pressure tolerances of early embryos in the deep-sea asteroid Plutonaster bifrons. J Mar Biol Assoc UK 76:749–757

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by National Science Foundation grant OCE-0118733 to C.M.Y. S.M.A. was supported by a National Science Foundation Graduate Research Fellowship and a Ford Foundation Pre-doctoral Fellowship. C. R. Fisher and R. S. Carney generously donated ship and submersible time and C. R. Fisher provided some live “Bathymodiolus” childressi samples. We gratefully acknowledge S. Brooke, A. L. Van Gaest, T. Smart, M. Wolf, and M. Holmes for helping to maintain mussels in the laboratory and S. Mills for proofreading the final draft of this manuscript. The suggestions of two anonymous reviewers and H.O. Portner greatly improved this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shawn M. Arellano.

Additional information

Communicated by H. O. Pörtner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arellano, S.M., Young, C.M. Temperature and salinity tolerances of embryos and larvae of the deep-sea mytilid mussel “Bathymodioluschildressi . Mar Biol 158, 2481–2493 (2011). https://doi.org/10.1007/s00227-011-1749-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1749-9

Keywords

Navigation