Marine Biology

, 163:218 | Cite as

Eastern oyster, Crassostrea virginica, valve gape behavior under diel-cycling hypoxia

Original paper

Abstract

Hypoxia and anoxia in many estuaries worldwide can cause a wide range of negative effects on animals that are directly exposed or indirectly influenced by food web interactions. Typically, experimental studies focus on animal behavior as a function of continuous exposure to low dissolved oxygen (DO) conditions rather than short-term fluctuations. Dissolved oxygen concentrations [DO] can, however, vary throughout the day, and water can become hypoxic for minutes to hours, often during the late night/early morning hours in the summer. Valve gape of 1-year-old eastern oysters, Crassostrea virginica, from Maryland, USA, was continuously measured while exposed to diel-cycling DO in aquaria during normoxic, hypoxic, and supersaturated phases of the cycle over several 2-day periods (July–August 2012). Severe hypoxia (0.6 mg DO L−1) induced oysters to close for significantly longer times than normoxic (7.3 mg DO L−1) conditions. Oysters exposed to mild hypoxia (1.7 mg DO L−1) closed for a similar amount of time as oysters held at normoxia and severe hypoxia. At severe hypoxia, more than one-third of the oysters closed simultaneously and closed immediately when they encountered severe hypoxia while oysters at mild hypoxia often closed later in the low oxygen phase of the cycles. When normoxia was reintroduced after severe hypoxia, most oysters opened immediately and gaped throughout the period. The results indicate that while 1-year-old oysters responded negatively to diel-cycling low [DO], especially to severe hypoxia, they rapidly opened during the normoxic period that followed, potentially reducing any negative effects of a fluctuating environment.

Keywords

Dissolve Oxygen Bivalve Severe Hypoxia Valve Closure Crassostrea Virginica 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Andrew Keppel, Virginia Clark, and Rebecca Burrell for maintaining the diel cycling hypoxia conditions throughout this experiment. We thank F. Scott Porter who built the valve gape apparatus. Oysters were purchased from Marinetics, Cambridge, Maryland. The hypoxia experiments were funded by a National Oceanic and Atmospheric Administration – Center for Sponsored Coastal Ocean Research grant No. NA10NOS4780138 and by the Smithsonian Hunterdon Fund to Denise Breitburg. The valve gape measurements during the hypoxia experiments were funded by a Faculty Enhancement Grant by Washington College to Elka T. Porter. We would also like to thank three anonymous reviewers for valuable suggestions that improved the manuscript.

Compliance with ethical standards

Conflict of interest

Author Elka T. Porter declares that she has no conflict of interest. Author Denise L. Breitburg declares that she has no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

227_2016_2980_MOESM1_ESM.pdf (23 kb)
Supplementary material 1 (PDF 23 kb)

References

  1. Altieri AH, Gedan KB (2015) Climate change and dead zones. Glob Change Biol 21:1395–1406. doi: 10.1111/gcb.12754 CrossRefGoogle Scholar
  2. Basti L, Nagai K, Shimasaki Y, Oshima Y, Honjo T, Segawa S (2009) Effects of the toxic dinoflagellate Heterocapsa circularisquama on the valve movement behaviour of the Manila clam Ruditapes philippinarum. Aquaculture 291:41–47. doi: 10.1016/j.aquaculture.2009.02.029 CrossRefGoogle Scholar
  3. Baumann H, Wallace RB, Tagliaferri T, Gobler CJ (2015) Large natural pH, CO2 and O2 fluctuations in a temperate tidal salt marsh on diel, seasonal, and interannual time scales. Estuaries Coast 38:220–231. doi: 10.1007/s12237-014-9800-y CrossRefGoogle Scholar
  4. Borcherding J (2006) Ten years of practical experience with the Dreissena-monitor, a biological early warning system for continuous water quality monitoring. Hydrobiologia 556:417–426. doi: 10.1007/s10750-005-1203-4 CrossRefGoogle Scholar
  5. Breitburg DL (1990) Near-shore hypoxia in the Chesapeake Bay: patterns and relationships among physical factors. Estaur Coast Shelf Sci 30:593–609CrossRefGoogle Scholar
  6. Breitburg D (2002) Effects of hypoxia, and the balance between hypoxia and enrichment on coastal fishes and fisheries. Estuaries 25:767–781CrossRefGoogle Scholar
  7. Breitburg DL, Hondorp D, Audemard C, Carnegie RB, Burrell RB, Trice M, Clark V (2015) Landscape-level variation in disease susceptibility related to shallow-water hypoxia. PLoS One 10:e0116223. doi: 10.1371/journal.pone.0116223 CrossRefGoogle Scholar
  8. Brown F (1954) Persistent activity rhythms in the oyster. Am J Physiol 178:510–514Google Scholar
  9. Burnett LE, Stickle WB (2001) Physiological responses to hypoxia. In: Rabelais NN, Turner RE (eds) Coastal hypoxia: consequences for living resources and ecosystems. coastal and Estuarine Studies 58. American Geophysical Union, Washington, DC, pp 101–114CrossRefGoogle Scholar
  10. Burrell RB, Keppel AG, Clark VM, Breitburg DL (2015) An automated monitoring and control system for flow-through co-cycling hypoxia and pH experiments. Limnol Oceanogr Methods. doi: 10.1002/lom3.10077 Google Scholar
  11. Clark V (2014) The effects of diel-cycling hypoxia and hypercapnia on eastern oyster, Crassostrea virginica (Gmelin), clearance rates and hemolymph pH. University of Maryland, College Park, Master of ScienceGoogle Scholar
  12. Comeau LA, Mayrand E, Mallet A (2012) Winter quiescence and spring awakening of the Eastern oyster Crassostrea virginica at its northernmost distribution limit. Mar Biol 159:2269–2279. doi: 10.1007/s00227-012-2012-8 CrossRefGoogle Scholar
  13. Costantini M, Ludsin SA, Mason DM, Zhang X, Boicourt WC, Brandt SB (2008) Effect of hypoxia on habitat quality of striped bass (Morone saxatilis) in Chesapeake Bay. Can J Fish Aquat Sci 65:989–1002. doi: 10.1139/f08-021 CrossRefGoogle Scholar
  14. Cranford PJ, Evans DA, Shumway SE (2011) Bivalve filter feeding: variability and limits of the aquaculture biofilter. In: Shumway S (ed) Shellfish aquaculture and the environment. Wiley, Oxford, pp 81–124CrossRefGoogle Scholar
  15. Curtis TM, Williamson R, Depledge MH (2000) Simultaneous, long term monitoring of valve and cardiac activity in the blue mussel Mytilus edulis exposed to copper. Mar Biol 136:837–846CrossRefGoogle Scholar
  16. Dame RF, Patten BC (1981) Analysis of energy flows in an intertidal oyster reef. Mar Ecol Prog Ser 5:115–124CrossRefGoogle Scholar
  17. de Zwart D, Kramer JM, Jenner HA (1995) Practical experiences with the biological early warning system “mosselmonitor”. Environ Toxicol Water 10:237–247CrossRefGoogle Scholar
  18. Dharmamaraj S (1983) Oxygen consumption in Pearl oyster Pinctada fucata (Gould) and Pinctada sugillata (Reeve). Proc Symp Coast Aquac 2:627–632Google Scholar
  19. Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr Mar Biol Ann Rev 33:245–303Google Scholar
  20. Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929CrossRefGoogle Scholar
  21. Dowd WW, Somero GN (2013) Behavior and survival of Mytilus congeners following episodes of elevated body temperature in air and seawater. J Exp Biol 216:502–514. doi: 10.1242/jeb.076620 CrossRefGoogle Scholar
  22. Famme P (1980) Effect of shell valve closure by the mussel Mytilus edulis L. on the rate of oxygen consumption in declining oxygen tension. Comp Biochem Physiol 67a:167–170CrossRefGoogle Scholar
  23. Galtsoff PS (1928) Experimental study of the function of the oyster gills and its bearing on the problems of oyster culture and sanitary control of the oyster industry. Bull US Bur Fish 44:1–39Google Scholar
  24. Gamenick I, Jahn A, Vopel K, Giere O (1996) Hypoxia and sulphide as structuring factors in a macrozoobenthic community on the Baltic Sea shore: colonization studies and tolerance experiments. Mar Ecol Prog Ser 144:73–85CrossRefGoogle Scholar
  25. Gnyubkin VF (2009) An early warning system for aquatic environment state monitoring based on an analysis of mussel valve movements. Russ J Mar Biol 35:431–436CrossRefGoogle Scholar
  26. Gooday AJ, Levin LA, Aranda da Silva A, Bett BJ, Cowie GL, Dissard D, Gage JD, Hughes DJ, Jeffreys R, Lamont PA, Larkin KE, Murty SJ, Schumacher S, Whitcraft C, Woulds C (2009) Faunal responses to oxygen gradients on the Pakistan margin: a comparison of foraminiferans, macrofauna and megafauna. Deep Sea Res Part II 56:488–502. doi: 10.1016/j.dsr2.2008.10.003 CrossRefGoogle Scholar
  27. Higgins PJ (1980) Effects of food availability on the valve movements and feeding behavior of juvenile Crassostrea virginica (Gmelin). I. Valve movements and periodic activity. J Exp Mar Biol Ecol 45:229–244CrossRefGoogle Scholar
  28. Huey RB, Bennett AF (1990) Physiological adjustments to fluctuating thermal environments: an ecological and evolutionary perspective. In: Morimoto R, Tissieres A, Georgopoulous C (eds) The role of heat shock and stress response in biology and human disease. Cold Harbor Laboratory Press, New York, pp 37–59Google Scholar
  29. Ivanina AV, Kurochkin IO, Leamy L, Sokolova IM (2012) Effects of temperature and cadmium exposure on the mitochondria of oysters (Crassostrea virginica) exposed to hypoxia and subsequent reoxygenation. J Exp Biol 215:3142–3154. doi: 10.1242/jeb.071357 CrossRefGoogle Scholar
  30. Jakubowska M, Normant M (2015) Metabolic rate and activity of blue mussel Mytilus edulis trossulus under short-term exposure to carbon dioxide-induced water acidification and oxygen deficiency. Mar Freshw Behav Physiol 48:25–39. doi: 10.1080/10236244.2014.986865 CrossRefGoogle Scholar
  31. Jakubowska M, Normant-Saremba M (2015) The effect of CO2-induced seawater acidification on the behaviour and metabolic rate of the Baltic clam Macoma balthica. Ann Zool Fenn 52:353–367. doi: 10.5735/086.052.0509 CrossRefGoogle Scholar
  32. Jansson A, Norkko J, Dupont S, Norkko A (2015) Growth and survival in a changing environment: combined effects of moderate hypoxia and low pH on juvenile bivalve Macoma balthica. J Sea Res 102:41–47. doi: 10.1016/j.seares.2015.04.006 CrossRefGoogle Scholar
  33. Jørgensen CB, Larsen P, Møhlenberg F, Riisgård HU (1988) The bivalve pump: properties and modelling. Mar Ecol Prog Ser 45:205–216CrossRefGoogle Scholar
  34. Kádár E, Salánki J, Judaosingh R, Powell JJ, McCrohan CR, White KN (2001) Avoidance responses to aluminum in the freshwater bivalve Anodonta cygnea. Aquat Toxicol 55:137–148CrossRefGoogle Scholar
  35. Keppel AG, Breitburg DL, Wikfors GH, Burrell RB, Clark VM (2015) Effects of co-varying diel-cycling hypoxia and pH on disease susceptibility in the eastern oyster Crassostrea virginica. Mar Ecol Prog Ser 538:169–183. doi: 10.3354/meps11479 CrossRefGoogle Scholar
  36. Levin LA, Breitburg DL (2015) Linking coasts and seas to address ocean deoxygenation. Nat Clim Change 5:401–403. doi: 10.1038/nclimate2595 CrossRefGoogle Scholar
  37. Llansó RJ (1992) Effects of hypoxia on estuarine benthos: the lower Rappahannock River (Chesapeake Bay), a case study. Estuar Coast Shelf Sci 35:491–515CrossRefGoogle Scholar
  38. Lombardi SA, Harlan NP, Paynter KT (2013) Survival, acid-base balance, and gaping responses of the Asian Oyster Crassostrea ariakensis and the Eastern Oyster Crassostrea virginica during clamped emersion and hypoxic immersion. J Shellfish Res 32:409–415. doi: 10.2983/035.032.0221 CrossRefGoogle Scholar
  39. Loosanoff VL (1962) Effects of turbidity on some larval and adult bivalves. In: Proceedings of the Fourteenth Gulf and Caribbean Fisheries Institute, Coral Gables, Florida USA, vol 14, pp 80–94Google Scholar
  40. Loosanoff VS, Nomejko CA (1946) Feeding of oysters in relation to tidal stages and to periods of light and darkness. Biol Bull (Woods Hole) 90:244–264CrossRefGoogle Scholar
  41. Ludsin SA, Zhang X, Brandt SB, Roman MR, Boicourt WC, Mason DM, Costantini M (2009) Hypoxia-avoidance by planktivorous fish in Chesapeake Bay: implications for food web interactions and fish recruitment. J Exp Mar Biol Ecol 381:S121–S131. doi: 10.1016/j.jembe.2009.07.016 CrossRefGoogle Scholar
  42. Modig H, Olafsson E (1998) Responses of Baltic benthic invertebrates to hypoxic events. J Exp Mar Biol Ecol 229:133–148CrossRefGoogle Scholar
  43. Montagna PA, Ritter C (2006) Direct and indirect effects of hypoxia on benthos in Corpus Christi Bay, Texas, U.S.A. J Exp Mar Biol Ecol 330:119–131. doi: 10.1016/j.jembe.2005.12.021 CrossRefGoogle Scholar
  44. Nicastro KR, Zardi GI, McQuaid CD, Stephens L, Radloff S, Blatch GL (2010) The role of gaping behaviour in habitat partitioning between coexisting intertidal mussels. BMC Ecol 10:17. doi: 10.1186/1472-6785-10-17 CrossRefGoogle Scholar
  45. Nicastro KR, Zardi GI, McQuaid CD, Pearson GA, Serrao EA (2012) Love thy neighbour: group properties of gaping behaviour in mussel aggregations. PLoS One 7(10):e47382CrossRefGoogle Scholar
  46. Ortmann C, Grieshaber MK (2003) Energy metabolism and valve closure behaviour in the Asian clam Corbicula fluminea. J Exp Biol 206:4167–4178. doi: 10.1242/jeb.00656 CrossRefGoogle Scholar
  47. Patterson HK, Boettcher A, Carmichael RH (2014) Biomarkers of dissolved oxygen stress in oysters: a tool for restoration and management efforts. PLoS One 9(8):e104440CrossRefGoogle Scholar
  48. Pynönnen KS, Huebner J (1995) Effects of episodic low pH exposure on the valve movements of the freshwater bivalve Anodonta cygnea L. Water Res 29:2579–2582CrossRefGoogle Scholar
  49. Riedel B, Zuschin M, Haselmair A, Stachowitsch M (2008) Oxygen depletion under glass: behavioural responses of benthic macrofauna to induced anoxia in the Northern Adriatic. J Exp Mar Biol Ecol 367:17–27. doi: 10.1016/j.jembe.2008.08.007 CrossRefGoogle Scholar
  50. Riedel B, Zuschin M, Stachowitsch M (2012) Tolerance of benthic macrofauna to hypoxia and anoxia in shallow coastal seas: a realistic scenario. Mar Ecol Prog Ser 458:39–52. doi: 10.3354/meps09724 CrossRefGoogle Scholar
  51. Riedel B, Pados T, Pretterebner K, Schiemer L, Steckbauer A, Haselmair A, Zuschin M, Stachowitsch M (2014) Effect of hypoxia and anoxia on invertebrate behaviour: ecological perspectives from species to community level. Biogeosciences 11:1491–1518. doi: 10.5194/bg-11-1491-2014 CrossRefGoogle Scholar
  52. Riisgård HU, Larsen PS (2015) Physiologically regulated valve-closure makes mussels long-term starvation survivors: test of hypothesis. J Molluscan Stud 81:303–307. doi: 10.1093/mollus/eyu087 CrossRefGoogle Scholar
  53. Riisgård HU, Lassen J, Kittner C (2006) Valve-gape response times in mussels (Mytilus edulis)-Effects of laboratory preceding-feeding conditions and in situ tidally induced variation in phytoplankton biomass. J Shellfish Res 25:901–911CrossRefGoogle Scholar
  54. Robson AA, De Leaniz CG, Wilson RP, Halsey LG (2010a) Behavioural adaptations of mussels to varying levels of food availability and predation risk. J Molluscan Stud 76:348–353. doi: 10.1093/mollus/eyq025 CrossRefGoogle Scholar
  55. Robson AA, de Leaniz CG, Wilson RP, Halsey LG (2010b) Effect of anthropogenic feeding regimes on activity rhythms of laboratory mussels exposed to natural light. Hydrobiologia 655:197–204. doi: 10.1007/s10750-010-0449-7 CrossRefGoogle Scholar
  56. Rodland DL, Schoene BR, Baier S, Zhang Z, Dreyer W, Page NA (2009) Changes in gape frequency, siphon activity and thermal response in the freshwater bivalves Anodonta cygnea and Margaritifera falcata. J Molluscan Stud 75:51–57. doi: 10.1093/mollus/eyn038 CrossRefGoogle Scholar
  57. Rovero F, Hughes RN, Chelazzi G (1999) Cardiac and behavioural responses of mussels to risk of predation by dogwhelks. Anim Behav 58:707–714CrossRefGoogle Scholar
  58. Scapini F (2014) Behaviour of mobile macrofauna is a key factor in beach ecology as response to rapid environmental changes. Estuar Coast Shelf Sci 150:36–44. doi: 10.1016/j.ecss.2013.11.001 CrossRefGoogle Scholar
  59. Shumway SE, Cucci TL (1987) The effects of the toxic dinoflagellate Protogonyaulax tamarensis on the feeding and behaviour of bivalve molluscs. Aquat Toxicol 10:9–27CrossRefGoogle Scholar
  60. Shumway SE, Koehn RK (1982) Oxygen consumption in the American oyster Crassostrea virginica. Mar Ecol Prog Ser 9:59–68CrossRefGoogle Scholar
  61. Soliman MFM, El-Shenawy NS, Tadros MM, Abd El-Azeez AA (2015) Impaired behavior and changes in some biochemical markers of bivalve (Ruditapes decussatus) due to zinc toxicity. Toxicol Environ Chem 97:674–686. doi: 10.1080/02772248.2015.1058381 CrossRefGoogle Scholar
  62. Sparks BL, Strayer DL (1998) Effects of low dissolved oxygen on juvenile Elliptio complanata (Bivalvia:Unionidae). J N Am Benthol Soc 17:129–134CrossRefGoogle Scholar
  63. Stickle WB, Kapper MA, Liu L-L, Gnaiger E, Wang SY (1989) Metabolic adaptations of several species of crustaceans and molluscs to hypoxia: tolerance and microcalometric studies. Biol Bull (Woods Hole) 177:303–312CrossRefGoogle Scholar
  64. Sussarellu R, Dudognon T, Fabioux C, Soudant P, Moraga D, Kraffe E (2013) Rapid mitochondrial adjustments in response to short-term hypoxia and re-oxygenation in the Pacific oyster, Crassostrea gigas. J Exp Biol 216:1561–1569. doi: 10.1242/jeb.075879 CrossRefGoogle Scholar
  65. Taylor AC (1976) The cardiac responses to shell opening and closure in the bivalve Arctica islandica (L.). J Exp Biol 64:751–759Google Scholar
  66. Tran D, Haberkorn H, Soudant P, Ciret P, Massabuau J-C (2010) Behavioral responses of Crassostrea gigas exposed to the harmful algae Alexandrium minutum. Aquaculture 298:338–345. doi: 10.1016/j.aquaculture.2009.10.030 CrossRefGoogle Scholar
  67. Tyler RM, Brady DC, Targett TE (2009) Temporal and spatial dynamics of diel-cycling hypoxia in estuarine tributaries. Estuaries Coast 32:123–145. doi: 10.1007/s12237-008-9108-x CrossRefGoogle Scholar
  68. Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proc Natl Acad Sci U S A 105:15452–15457. doi: 10.1073/pnas.0803833105 CrossRefGoogle Scholar
  69. Villnäs A, Norkko J, Lukkari K, Hewitt J, Norkko A (2012) Consequences of increasing hypoxic disturbance on benthic communities and ecosystem functioning. PLoS One 7:e44920. doi: 10.1371/journal.pone.0044920 CrossRefGoogle Scholar
  70. Zhang H, Ludsin SA, Mason DM, Adamack AT, Brandt SB, Zhang X, Kimmel DG, Roman MR, Boicourt WC (2009) Hypoxia-driven changes in the behavior and spatial distribution of pelagic fish and mesozooplankton in the northern Gulf of Mexico. J Exp Mar Biol Ecol 381:S80–S91. doi: 10.1016/j.jembe.2009.07.014 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Yale Gordon College of Arts and SciencesUniversity of BaltimoreBaltimoreUSA
  2. 2.Smithsonian InstitutionEdgewaterUSA

Personalised recommendations