Skip to main content
SpringerLink
Log in

Establishing the thermal window for aerobic scope in New Zealand geoduck clams (Panopea zelandica)

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Geoduck clams (Panopea spp.) are the longest-lived and largest deep burrowing bivalve. Their unique morphology allows them to live buried in the sediment at depths of up to 1 m. The endemic New Zealand geoduck (Panopea zelandica Quoy and Gaimard, 1835) has recently been identified as a potential species for aquaculture. However, very little is known about the biology and physiology of this entirely subtidal geoduck species. Currently, the New Zealand geoduck fishery relies entirely upon wild harvests, but farms are expected to emerge as cultivation protocols are established. A key step in the optimization of cultivation procedures is the identification of optimal temperature and food rations. One method for establishing thermal optima is to identify the temperature window that supports the widest aerobic scope: the degree to which metabolic rate can be increased to support elevated activity demands. Thus, we investigated the aerobic scope for activity at five different temperatures representative of typical environmental conditions (8, 11, 15, 19, and 23 °C) for juvenile and young adult P. zelandica. Clearance rate was also measured at all temperatures. Comparisons of aerobic scope for activity and clearance rates between size classes revealed that juvenile geoducks had a narrower thermal optimum than young adults (15–19 versus 11–19 °C, respectively). Temperatures higher than 19 °C resulted in a reduction of aerobic scope for activity and clearance rate for both juvenile and young adults, which may lead to reduced performance and elevated mortality. These findings provide the first measures of aerobic scope in P. zelandica, a key step towards a meaningful understanding of the ecophysiology of this unusual species.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Albentosa M, Beiras R, Camacho AP (1994) Determination of optimal thermal conditions for growth of clam (Venerupis pullastra) seed. Aquaculture 126:315–328. doi:10.1016/0044-8486(94)90048-5

    Article  Google Scholar 

  • Anestis A, Pörtner HO, Karagiannis D, Angelidis P, Staikou A, Michaelidis B (2010) Response of Mytilus galloprovincialis (L.) to increasing seawater temperature and to marteliosis: metabolic and physiological parameters. Comp Biochem Physiol A Mol Integr Physiol 156:57–66. doi:10.1016/j.cbpa.2009.12.018

    Article  PubMed  Google Scholar 

  • Arney B, Liu W, Forster I, Mckinley RS, Pearce CM (2015) Temperature and food-ration optimization in the hatchery culture of juveniles of the Pacific geoduck Panopea generosa. J Shellfish Res 34:39–53. doi:10.2983/035.034.0107

    Article  Google Scholar 

  • Bayne BL (2001) Reply to comment by H.U. Riisgård. Ophelia 54:211. doi:10.1080/00785236.2001.10409466

    Article  Google Scholar 

  • Bayne BL, Newell RC (1983) Physiological energetics of marine molluscs. In: Saleuddin ASM, Wilbur KM (eds) The Mollusca, vol 4., Physiology (Part 1)Academic Press, New York, pp 407–515

    Google Scholar 

  • Bayne BL, Thompson RJ, Widdows J (1976) Physiology: I. In: Bayne BL (ed) Marine mussels their ecology and physiology. Cambridge University Press, London, pp 121–206

    Google Scholar 

  • Beiras R, Camacho AP, Albentosa M (1994) Comparison of the scope for growth with the growth performance of Ostrea edulis seed reared at different food concentrations in an open-flow system. Mar Biol 119:227–233. doi:10.1007/BF00349561

    Article  Google Scholar 

  • Bendif EM, Probert I, Schroeder DC, de Vargas C (2013) On the description of Tisochrysis lutea gen. nov. sp. nov. and Isochrysis nuda sp. nov. in the Isochrysidales, and the transfer of Dicrateria to the Prymnesiales (Haptophyta). J Appl Phycol 25(6):1763–1776. doi:10.1007/s10811-013-0037-0

    Article  CAS  Google Scholar 

  • Bendif EM, Probert I, Schroeder DC, de Vargas C (2014) Erratum to: on the description of Tisochrysis lutea gen. nov. sp. nov. and Isochrysis nuda sp. nov. in the Isochrysidales, and the transfer of Dicrateria to the Prymnesiales (Haptophyta). J Appl Phycol 26:1617. doi:10.1007/s10811-014-0284-8

    Google Scholar 

  • Breen P, Gabriel C, Tyson T (1991) Preliminary estimates of age, mortality, growth, and reproduction in the Hiatellid clam Panopea zelandica in New Zealand. NZ J Mar Freshwat Res 25:231–237

    Article  Google Scholar 

  • Brokordt KB, Himmelman JH, Guderley HE (2000) Effect of reproduction on escape responses and muscle metabolic capacities in the scallop Chlamys islandica Müller 1776. J Exp Mar Biol Ecol 251:205–225. doi:10.1016/S0022-0981(00)00215-X

    Article  CAS  PubMed  Google Scholar 

  • Buxton CD, Newell RC, Field JG (1981) Response-surface analysis of the combined effects of exposure and acclimation temperatures on filtration, oxygen consumption and scope for growth in the oyster Ostrea edulis. Mar Ecol Prog Ser 6:73–82. doi:10.3354/meps006073

    Article  Google Scholar 

  • Campbell A, Harbo RM, Hand CM Harvesting and distribution of Pacific geoduck clams, Panopea abrupta, in British Columbia. In: Jamieson GS, Campbell A (eds) Proceedings of the North Pacific Symposium on Invertebrate Stock Assessment and Management, Ottawa, 1998. National Research Council of Canada Research Press, pp 349–358

  • Claireaux G, Lefrançois C (2007) Linking environmental variability and fish performance: integration through the concept of scope for activity. Philos Trans R Soc B Biol Sci 362:2031–2041. doi:10.1098/rstb.2007.2099

    Article  Google Scholar 

  • Coughlan J (1969) The estimation of filtering rate from the clearance of suspensions. Mar Biol 2:356–358. doi:10.1007/BF00355716

    Article  Google Scholar 

  • Crisp DJ (1971) Energy flow measurements. In: Holme NA, McIntyre AD (eds) Methods for the study of marine benthos. Blackwell, Oxford, pp 197–323

    Google Scholar 

  • Filgueira R, Labarta U, Fernandez-Reiriz MJ (2006) Flow-through chamber method for clearance rate measurements in bivalves: design and validation of individual chambers and mesocosm. Limnol Oceanogr Methods 4:284–292. doi:10.4319/lom.2006.4.284

    Article  Google Scholar 

  • Fry FEJ (1947) Effects of the environment on animal activity. In: University of Toronto Studies, Biological Series, No. 55, pp 2–62

  • Goodwin L (1976) Observations on spawning and growth of subtidal geoducks (Panopea generosa, Gould). Proc Natl Shellfish Assoc 65:49–58

    Google Scholar 

  • Goodwin CL, Pease B (1989) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Pacific Northwest)—Pacific Geoduck Clam United States of Fish and Wildlife Service. Biol Rep 82:1–14

    Google Scholar 

  • Gribben PE, Creese RG (2005) Age, growth, and mortality of the New Zealand geoduck clam, Panopea zelandica (Bivalvia: Hiatellidae) in two north island populations. Bull Mar Sci 77:119–135

    Google Scholar 

  • Gribben PE, Heasman KG (2015) Developing fisheries and aquaculture industries for Panopea zelandica in New Zealand. J Shellfish Research 34(1):5–10. doi:10.2983/035.034.0103

    Article  Google Scholar 

  • Gribben PE, Helson J, Jeffs AG (2004) Reproductive cycle of the New Zealand geoduck, Panopea zelandica, in two north island populations. Veliger 47:53–65

    Google Scholar 

  • Guzmán-Agüero JE, Nieves-Soto M, Hurtado MÁ, Piña-Valdez P, Garza-Aguirre MDC (2013) Feeding physiology and scope for growth of the oyster Crassostrea corteziensis (Hertlein, 1951) acclimated to different conditions of temperature and salinity. Aquacult Int 21:283–297. doi:10.1007/s10499-012-9550-4

    Article  Google Scholar 

  • Han KN, Lee SW, Wang SY (2008) The effect of temperature on the energy budget of the Manila clam, Ruditapes philippinarum. Aquacult Int 16:143–152. doi:10.1007/s10499-007-9133-y

    Article  Google Scholar 

  • Ibarrola I, Larretxea X, Navarro E, Iglesias JIP, Urrutia MB (2008) Effects of body-size and season on digestive organ size and the energy balance of cockles fed with a constant diet of phytoplankton. J Comp Physiol B 178:501–514. doi:10.1007/s00360-007-0243-7

    Article  CAS  PubMed  Google Scholar 

  • IPCC (2014) Climate change 2014: impacts, adaptation, and vulnerability. Part B: regional aspects. Contribution of working group ii to the fifth assessment report of the intergovernmental panel on climate change. Barros VR, Field CB, Dokken DJ, Mastrandrea MD, Mach KJ, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Cambridge University Press, Cambridge

  • Jobling M (1981) Temperature tolerance and the final preferendum-rapid methods for the assessment of optimum growth temperatures. J Fish Biol 19:439–455

    Article  Google Scholar 

  • Kinne O (1970) Temperature. In: Kinne O (ed) Marine ecology—environmental factors, vol 1. Wiley, London, pp 407–514. doi:10.1080/10417946609371849

    Google Scholar 

  • Kittner C, Riisgård HU (2005) Effect of temperature on filtration rate in the mussel Mytilus edulis: no evidence for temperature compensation. Mar Ecol Prog Ser 305:147–152. doi:10.3354/meps305147

    Article  Google Scholar 

  • Laing I, Utting SD, Kilada RWS (1987) Interactive effect of diet and temperature on the growth of juvenile clams. J Exp Mar Biol Ecol 113:23–38. doi:10.1016/0022-0981(87)90080-3

    Article  Google Scholar 

  • Larsen PS, Riisgård HU (2009) Viscosity and not biological mechanisms often controls the effects of temperature on ciliary activity and swimming velocity of small aquatic organisms. J Exp Mar Biol Ecol 381:67–73. doi:10.1016/j.jembe.2009.09.021

    Article  Google Scholar 

  • Le Gall J-L, Raillard O (1988) Influence de la température sur la physiologie de l’huître Crassostrea gigas. Oceanis 14:603–608

    Google Scholar 

  • Le DV, Alfaro AC, King N (2014) Broodstock conditioning of New Zealand geoduck (Panopea zelandica) within different temperature and feeding ration regimes. NZ J Mar Freshw Res 48:356–370. doi:10.1080/00288330.2014.918548

    Article  Google Scholar 

  • Le DV, Alfaro AC, Ragg NLC, Hilton Z, King N (2016) Aerobic scope and oxygen regulation of New Zealand geoduck (Panopea zelandica) in response to progressive hypoxia. Aquaculture 463:28–36

    Article  Google Scholar 

  • Lurman GJ, Hilton Z, Ragg LCN (2013) Energetics of byssus attachment and feeding in the green-lipped mussel Perna canaliculus. Biol Bull 224:79–88

    Article  PubMed  Google Scholar 

  • Lurman G, Walter J, Hoppeler HH (2014a) Seasonal changes in the behaviour and respiration physiology of the freshwater duck mussel, Anodonta anatina. J Exp Biol 217:235–243. doi:10.1242/jeb.093450

    Article  PubMed  Google Scholar 

  • Lurman GJ, Walter J, Hoppeler HH (2014b) The effect of seasonal temperature variation on behaviour and metabolism in the freshwater mussel (Unio tumidus). J Therm Biol 43:13–23. doi:10.1016/j.jtherbio.2014.04.005

    Article  PubMed  Google Scholar 

  • Morley SA, Peck LS, Miller AJ, Pörtner HO (2007) Hypoxia tolerance associated with activity reduction is a key adaptation for Laternula elliptica seasonal energetics. Oecologia 153:29–36. doi:10.1007/s00442-007-0720-4

    Article  PubMed  Google Scholar 

  • Moullac GL, Quéau I, Souchu PL, Pouvreau S, Moal J, Coz JRL, Samain JF (2007) Metabolic adjustments in the oyster Crassostrea gigas according to oxygen level and temperature. Mar Biol Res 3:357–366. doi:10.1080/17451000701635128

    Article  Google Scholar 

  • Norkko J, Pilditch CA, Thrush SF, Wells RMG (2005) Effects of food availability and hypoxia on bivalves: the value of using multiple parameters to measure bivalve condition in environmental studies. Mar Ecol Prog Ser 298:205–218

    Article  Google Scholar 

  • Orensanz JM, Hand CM, Parma AM, Valero J, Hilborn R (2004) Precaution in the harvest of Methuselah’s clams—the difficulty of getting timely feedback from slow-paced dynamics. Can J Fish Aquat Sci 61(8):1355–1372. doi:10.1139/f04-136

    Article  Google Scholar 

  • Peck LS, Webb KE, Bailey DM (2004) Extreme sensitivity of biological function to temperature in Antarctic marine species. Funct Ecol 18:625–630

    Article  Google Scholar 

  • Peck LS, Morley SA, Pörtner HO, Clark MS (2007) Thermal limits of burrowing capacity are linked to oxygen availability and size in the Antarctic clam Laternula elliptica. Oecologia 154(3):479–484. doi:10.1007/s00442-007-0858-0

    Article  PubMed  Google Scholar 

  • Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692. doi:10.1126/science.1163156

    Article  PubMed  Google Scholar 

  • Pörtner HO, Peck MA (2010) Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. J Fish Biol 77:1745–1779. doi:10.1111/j.1095-8649.2010.02783.x

    Article  PubMed  Google Scholar 

  • Pörtner HO et al (2014) How and how not to investigate the oxygen and capacity limitation of thermal tolerance (OCLTT) and aerobic scope—remarks on the article by Gräns. J Exp Biol 217(24):4432–4433. doi:10.1242/jeb.114181

    Article  PubMed  Google Scholar 

  • Riisgård HU (2001) On measurement of filtration rate in bivalves-the stony road to reliable data: review and interpretation. Mar Ecol Prog Ser 211:275–291. doi:10.3354/meps211275

    Article  Google Scholar 

  • Schalkhausser B, Bock C, Pörtner H-O, Lannig G (2014) Escape performance of temperate king scallop, Pecten maximus under ocean warming and acidification. Mar Biol 161(12):2819–2829. doi:10.1007/s00227-014-2548-x

    Article  CAS  Google Scholar 

  • Schulte PM (2015) The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment. J Exp Biol 218(Pt 12):1856–1866. doi:10.1242/jeb.118851

    Article  PubMed  Google Scholar 

  • Sgro L, Munari C, Angonese A, Basso S, Mistri M (2005) Functional responses and scope for growth of two non-indigenous bivalve species in the Sacca di Goro (northern Adriatic Sea, Italy). Ital J Zool 72:235–239. doi:10.1080/11250000509356677

    Article  Google Scholar 

  • Sicard MT, Maeda-Martinez AN, Lluch-Cota SE, Lodeiros C, Roldan-Carrillo LM, Mendoza-Alfaro R (2006) Frequent monitoring of temperature: an essential requirement for site selection in bivalve aquaculture in tropical-temperate transition zones. Aquac Res 37:1040–1049. doi:10.1111/j.1365-2109.2006.01527.x

    Article  Google Scholar 

  • Sobral P, Widdows J (1997) Influence of hypoxia and anoxia on the physiological responses of the clam Ruditapes decussatus from southern Portugal. Mar Biol 127:455–461. doi:10.1007/s002270050033

    Article  Google Scholar 

  • Sokolova IM, Pörtner H-O (2003) Metabolic plasticity and critical temperatures for aerobic scope in a eurythermal marine invertebrate (Littorina saxatilis, Gastropoda: Littorinidae) from different latitudes. J Exp Biol 206(1):195–207. doi:10.1242/jeb.00054

    Article  PubMed  Google Scholar 

  • Sunday JM, Bates AE, Dulvy NK (2011) Global analysis of thermal tolerance and latitude in ectotherms. Proc R Soc B Biol Sci 278:1823–1830. doi:10.1098/rspb.2010.1295

    Article  Google Scholar 

  • Sunday JM, Bates AE, Dulvy NK (2012) Thermal tolerance and the global redistribution of animals. Nat Clim Change 2:686–690. doi:10.1038/nclimate1539

    Article  Google Scholar 

  • Tamayo D, Ibarrola I, Navarro E (2013) Thermal dependence of clearance and metabolic rates in slow- and fast-growing spats of manila clam Ruditapes philippinarum. J Comp Physiol B 183:893–904. doi:10.1007/s00360-013-0764-1

    Article  PubMed  Google Scholar 

  • Thompson RJ, Bayne BL (1972) Active metabolism associated with feeding in the mussel Mytilus edulis L. J Exp Mar Biol Ecol 9:111–124. doi:10.1016/0022-0981(72)90011-1

    Article  CAS  Google Scholar 

  • Verberk WCEP, Bilton DT (2013) Respiratory control in aquatic insects dictates their vulnerability to global warming. Biol Lett 9(2013047):1–4

    Google Scholar 

  • Wang WX, Widdows J (1993) Calorimetric studies on the energy metabolism of an infaunal bivalve, Abra tenuis, under normoxia, hypoxia and anoxia. Mar Biol 116:73–79. doi:10.1007/bf00350733

    Article  Google Scholar 

  • Watson SA, Morley SA, Bates AE, Clark MS, Day RW, Lamare M, Martin SM, Southgate PC, Tan KS, Tyler PA, Peck LS (2014) Low global sensitivity of metabolic rate to temperature in calcified marine invertebrates. Oecologia 174:45–54. doi:10.1007/s00442-013-2767-8

    Article  PubMed  Google Scholar 

  • Widdows J (1973) The effects of temperature on the metabolism and activity of Mytilus edulis. Neth J Sea Res 7:387–398. doi:10.1016/0077-7579(73)90060-4

    Article  Google Scholar 

  • Winter JE (1978) A review on the knowledge of suspension-feeding in lamellibranchiate bivalves, with special reference to artificial aquaculture systems. Aquaculture 13:1–33. doi:10.1016/0044-8486(78)90124-2

    Article  Google Scholar 

Download references

Acknowledgments

This project was funded by the Cawthron Cultured Shellfish Programme (NZ Ministry of Business, Innovation and Employment contracts CAWS0802, CAW1315). Logistical and technical support was provided by the School of Applied Sciences, Auckland University of Technology (AUT). We are grateful to the Aquaculture Biotechnology Group at AUT for fruitful discussions that improved this research. This project is part of a Ph.D. thesis, which was supported by a New Zealand Aid scholarship awarded to D.V. Le under the supervision of A.C. Alfaro.

Author information

Authors and Affiliations

  1. Institute for Applied Ecology New Zealand, School of Sciences, Faculty of Health and Environmental Sciences, Auckland University of Technology, Private Bag 92006, Auckland, 1142, New Zealand

    Dung V. Le & Andrea C. Alfaro

  2. Cawthron Institute, Nelson, New Zealand

    Norman L. C. Ragg, Zoë Hilton & Nick King

  3. Center of Aquaculture Biotechnology, Research Institute for Aquaculture No.1, Bac Ninh, Vietnam

    Dung V. Le

Authors
  1. Dung V. Le
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea C. Alfaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Norman L. C. Ragg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zoë Hilton
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nick King
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea C. Alfaro.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Le, D.V., Alfaro, A.C., Ragg, N.L.C. et al. Establishing the thermal window for aerobic scope in New Zealand geoduck clams (Panopea zelandica). J Comp Physiol B 187, 265–276 (2017). https://doi.org/10.1007/s00360-016-1038-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-016-1038-5

Keywords

Search

Navigation