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Advances in the aquatic sciences
RESEARCH ARTICLE (Open Access)

Effects of acclimation temperature and exposure time on the scope for growth of the blackfoot Pāua (Haliotis iris)

Thuy T. Nguyen https://orcid.org/0009-0009-6532-3795 A B * , Islay D. Marsden A , William Davison A and John Pirker A
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch 8020, New Zealand.

B Department of Fisheries, Ministry of Agriculture and Rural Development, 10 Nguyen Cong Hoan, Ba Dinh, Ha Noi, Vietnam.

* Correspondence to: tng35@uclive.ac.nz

Handling Editor: Lauren Nadler

Marine and Freshwater Research 74(17) 1465-1477 https://doi.org/10.1071/MF23131
Submitted: 7 July 2023  Accepted: 17 October 2023  Published: 13 November 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

Climate change and increased seawater temperatures can greatly affect physiological processes and growth of marine ectotherms, including the blackfoot haliotid, Pāua (Haliotis iris). Scope for growth (SFG) is a laboratory-derived measure of the energy available for growth but this has not been examined in Pāua.

Aims

To measure SFG of seasonally collected Pāua and their haemolymph parameters at constant acclimation temperatures of 12, 15, 18 and 21°C for 28 days.

Methods

Energy available for growth was measured from kelp food and losses due to respiration and ammonia excretion calculated on Days 1, 14, 21 and 28 of acclimation. Haemolymph parameters were also measured.

Key results

After 3 days of acclimation, SFG was highly variable. Following 2 weeks of acclimation, SFG was positive for all temperatures. Respiration and excretion energies depended on both acclimation temperature and time. Haemolymph parameters were affected by acclimation temperature.

Conclusion

Pāua have limited ability to acclimate to a temperature 21°C suggesting that they would not grow effectively at this temperature.

Implications

This research suggests that adult Pāua can be adversely affected by increased seawater temperature, resulting from climate change and this could affect their future growth and distribution.

Keywords: acclimation capacity, biochemistry, energy, global warming, haemolymph, Haliotis iris, Pāua, physiology.

References

Aalto EA, Barry JP, Boch CA, Litvin SY, Micheli F, Woodson CB, De Leo GA (2020) Abalone populations are most sensitive to environmental stress effects on adult individuals. Marine Ecology Progress Series 643, 75-85.
| Crossref | Google Scholar |

Alter K, Andrewartha SJ, Morash AJ, Clark TD, Hellicar AD, León RI, Elliott NG (2017) Hybrid abalone are more robust to multi-stressor environments than pure parental species. Aquaculture 478, 25-34.
| Crossref | Google Scholar |

Arafeh-Dalmau N, Montaño-Moctezuma G, Martinez JA, Beas-Luna R, Schoeman DS, Torres-Moye G (2019) Extreme marine heatwaves alter kelp forest community near its equatorward distribution limit. Frontiers in Marine Science 6, 499.
| Crossref | Google Scholar |

Baillieul M, Selens M, Blust R (1996) Scope for growth and fitness of daphnia magna in salinity-stressed conditions. Functional Ecology 10(2), 227-233.
| Crossref | Google Scholar |

Bansemer MS, Qin JG, Harris JO, Duong DN, Hoang TH, Howarth GS, Stone DAJ (2016) Growth and feed utilisation of greenlip abalone (Haliotis laevigata) fed nutrient enriched macroalgae. Aquaculture 452, 62-68.
| Crossref | Google Scholar |

Barkai R, Griffiths CL (1987) Consumption, absorption efficiency, respiration and excretion in the South African abalone Haliotis midae. South African Journal of Marine Science 5(1), 523-529.
| Crossref | Google Scholar |

Barkai R, Griffiths CL (1988) An energy budget for the South African abalone Haliotis midae Linnaeus. Journal of Molluscan Studies 54(1), 43-51.
| Crossref | Google Scholar |

Bayne BL, Newell RC (1983) Physiological energetics of marine molluscs. In ‘The Mollusca’. (Eds ASM Saleuddin, KM Wilbur) pp. 407–515. (Academic Press: Cambridge, MA, USA) doi:10.1016/B978-0-12-751404-8.50017-7

Behrens JW, Elias JP, Taylor HH, Weber RE (2002) The archaeogastropod mollusc Haliotis iris: tissue and blood metabolites and allosteric regulation of haemocyanin function. Journal of Experimental Biology 205, 253-263.
| Crossref | Google Scholar | PubMed |

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. Marine Biology 119(2), 227-233.
| Crossref | Google Scholar |

Borecka A, Janas U, Kendzierska H (2016) The combined effect of temperature and salinity changes on osmoregulation and haemocyanin concentration in Saduria entomon (Linnaeus, 1758). Marine Biology Research 12(3), 316-322.
| Crossref | Google Scholar |

Britz PJ, Hecht T, Mangold S (1997) Effect of temperature on growth, feed consumption and nutritional indices of Haliotis midae fed a formulated diet. Aquaculture 152(1–4), 191-203.
| Crossref | Google Scholar |

Conover RJ (1966) Assimilation of organic matter by zooplankton. Limnology and Oceanography 11(3), 338-345.
| Crossref | Google Scholar |

Cossins AR, Bowler K (1987) ‘Temperature biology of animals.’ (Chapman and Hall: London, British)

Day R, Hooper C, Benkendorff K, Slocombe R, Handlinger J (2010) Investigations on the immunology of stressed abalone. Project Number 2004/233. (University of Melbourne: Melbourne, Vic., Australia) Available at https://www.frdc.com.au/sites/default/files/products/2004-233-DLD.pdf

Einarson S (1993) Effects of temperature, seawater osmolality and season on oxygen consumption and osmoregulation of the amphipod Gammarus oceanicus. Marine Biology 117(4), 599-606.
| Crossref | Google Scholar |

Elliot JM, Davison W (1975) Energy equivalents of oxygen consumption in animal energetics. Oecologia 201, 195-201.
| Crossref | Google Scholar |

Farías A, García-Esquivel Z, Viana MT (2003) Physiological energetics of the green abalone, Haliotis fulgens, fed on a balanced diet. Journal of Experimental Marine Biology and Ecology 289(2), 263-276.
| Crossref | Google Scholar |

Fredrick WS, Ravichandran S (2012) Hemolymph proteins in marine crustaceans. Asian Pacific Journal of Tropical Biomedicine 2(6), 496-502.
| Crossref | Google Scholar | PubMed |

Ganmanee M, Sirirustananun N, Jarayabhand P (2010) Energy budget of the thai abalone Haliotis asinina reared in a semiclosed recirculating land-based system. Journal of Shellfish Research 29(3), 637-642.
| Crossref | Google Scholar |

Genoni GP, Pahl-Wostl C (1991) Measurement of scope for change in ascendency for short-term assessment of community stress. Canadian Journal of Fisheries and Aquatic Sciences 48, 968-974.
| Crossref | Google Scholar |

Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293, 2248-2251.
| Crossref | Google Scholar | PubMed |

Giomi F, Pörtner H-O (2013) A role for haemolymph oxygen capacity in heat tolerance of eurythermal crabs. Frontiers in Physiology 4, 110.
| Crossref | Google Scholar |

González ML, López DA, Pérez MC, Castro JM (2002) Effect of temperature on the scope for growth in juvenile scallops Argopecten purpuratus (Lamark, 1819). Aquaculture International 10(4), 339-348.
| Crossref | Google Scholar |

González GG, Brokordt KB, Winkler FE (2010) Repeatability of physiological traits in juvenile Pacific abalone, Haliotis discus hannai. Marine Biology 157(10), 2195-2203.
| Crossref | Google Scholar |

Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biological Reviews 74(1), 1-40.
| Crossref | Google Scholar | PubMed |

Haist V (2018) Analysis of paua maturity and growth. New Zealand Fisheries Assessment Report 2018/21. Available at https://fs.fish.govt.nz/Doc/24606/FAR-2018-21-Paua-Maturity-and-Growth.pdf.ashx

Harris JO, Maguire GB, Edwards SJ, Johns DR (1999) Low dissolved oxygen reduces growth rate and oxygen consumption rate of juvenile greenlip abalone, Haliotis laevigata Donovan. Aquaculture 174, 265-278.
| Crossref | Google Scholar |

Hawkins AJS (1995) Effects of temperature change on ectotherm metabolism and evolution: metabolic and physiological interrelations underlying the superiority of multi-locus heterozygotes in heterogeneous environments. Journal of Thermal Biology 20(1–2), 23-33.
| Crossref | Google Scholar |

Hawkins AJS, Duarte P, Fang JG, Pascoe PL, Zhang JH, Zhang XL, Zhu MY (2002) A functional model of responsive suspension-feeding and growth in bivalve shellfish, configured and validated for the scallop Chlamys farreri during culture in China. Journal of Experimental Marine Biology and Ecology 281, 13-40.
| Crossref | Google Scholar |

Hernández-Sandoval P, Díaz F, Re-Araujo AD, López-Sánchez JA, Martínez-Valenzuela MDC, García-Guerrero M, Rosas C (2018) Thermal preference, critical thermal limits, oxygen routine consumption and active metabolic scope of Macrobrachium tenellum (Smith, 1871) maintained at different acclimation temperatures. Latin American Journal of Aquatic Research 46(3), 558-569.
| Crossref | Google Scholar |

Hildreth JE, Stickle WB (1980) The effects of temperature and salinity on the osmotic composition of the Southern oyster drill, Thais Haemastoma. The Biological Bulletin 159(1), 148-161.
| Crossref | Google Scholar |

Hooker SH, Creese RG, Jeffs AG (1997) Growth and demography of paua Haliotis iris (Mollusca: Gastropoda) in northeastern New Zealand. Molluscan Research 18, 299-311.
| Crossref | Google Scholar |

Hooper C, Day R, Slocombe R, Handlinger J, Benkendorff K (2007) Stress and immune responses in abalone: limitations in current knowledge and investigative methods based on other models. Fish & Shellfish Immunology 22(4), 363-379.
| Crossref | Google Scholar | PubMed |

Hooper C, Day R, Slocombe R, Benkendorff K, Handlinger J, Goulias J (2014) Effects of severe heat stress on immune function, biochemistry and histopathology in farmed Australian abalone (hybrid Haliotis laevigata × Haliotis rubra). Aquaculture 432, 26-37.
| Crossref | Google Scholar |

Jaenicke E, Fraune S, May S, Irmak P, Augustin R, Meesters C, Decker H, Zimmer M (2009) Is activated hemocyanin instead of phenoloxidase involved in immune response in woodlice? Developmental & Comparative Immunology 33(10), 1055-1063.
| Crossref | Google Scholar | PubMed |

Kang HY, Lee Y-J, Lee Y-J, Song W-Y, Kim T-I, Lee W-C, Kim TY, Kang C-K (2019) Physiological responses of the abalone Haliotis discus hannai to daily and seasonal temperature variations. Scientific Reports 9(1), 8019.
| Crossref | Google Scholar |

Kong N, Liu X, Li J, Mu W, Lian J, Xue Y, Li Q (2017) Effects of temperature and salinity on survival, growth and DNA methylation of juvenile Pacific abalone, Haliotis discus hannai Ino. Chinese Journal of Oceanology and Limnology 35(5), 1248-1258.
| Crossref | Google Scholar |

Lamare MD, Wing SR (2001) Calorific content of New Zealand marine macrophytes. New Zealand Journal of Marine and Freshwater Research 35, 335-341.
| Crossref | Google Scholar |

Lopez LM, Tyler P (2006) Energy budget of cultured female abalone Haliotis tuberculata (L.). Journal of Shellfish Research 25(2), 385-389.
| Crossref | Google Scholar |

Lu Y, Wang F, Li L, Dong S (2016) Responses of metabolism and haemolymph ions of swimming crab Portunus trituberculatus to thermal stresses: a comparative study between air and water. Aquaculture Research 47(9), 2989-3000.
| Crossref | Google Scholar |

Mardones ML, Thatje S, Fenberg PB, Hauton C (2022) The short and long-term implications of warming and increased sea water pCO2 on the physiological response of a temperate neogastropod species. Marine Biology 169,, 3.
| Crossref | Google Scholar |

Markle TM, Kozak KH (2018) Low acclimation capacity of narrow-ranging thermal specialists exposes susceptibility to global climate change. Ecology and Evolution 8, 4644-4656.
| Crossref | Google Scholar | PubMed |

Mayzaud P, Conover RJ (1988) O:N atomic ratio as a tool to describe zooplankton metabolism. Marine Ecology Progress Series 45, 289-302.
| Crossref | Google Scholar |

McBride SC, Rotem E, Ben-Ezra D, Shpigel M (2001) Seasonal energetics of Haliotis fulgens (Philippi) and Haliotis tuberculata (L.). Journal of Shellfish Research 20(2), 659-665.
| Google Scholar |

Morash AJ, Alter K (2016) Effects of environmental and farm stress on abalone physiology: perspectives for abalone aquaculture in the face of global climate change. Reviews in Aquaculture 8, 342-368.
| Crossref | Google Scholar |

Mubiana VK, Blust R (2007) Effects of temperature on scope for growth and accumulation of Cd, Co, Cu and Pb by the marine bivalve Mytilus edulis. Marine Environmental Research 63(3), 219-235.
| Crossref | Google Scholar | PubMed |

Navarro JM, Leiva GE, Gallardo CS, Varela C (2002) Influence of diet and temperature on physiological energetics of Chorus giganteus (Gastropoda: Muricidae) during reproductive conditioning. New Zealand Journal of Marine and Freshwater Research 36(2), 321-332.
| Crossref | Google Scholar |

Naylor JR, Andrew NL (2004) Productivity and response to fishing of stunted paua stocks. New Zealand Fisheries Assessment Report 2004B1. (Ministry of Fisheries) Available at https://docs.niwa.co.nz/library/public/FAR2004-31.pdf

Naylor JR, Andrew NL, Kim SW (2006) Demographic variation in the New Zealand abalone Haliotis iris. Marine and Freshwater Research 57(2), 215-224.
| Crossref | Google Scholar |

Oliveira GF, Siregar H, Queiroga H, Peteiro LG (2021) Main drivers of fecundity variability of mussels along a latitudinal gradient: lessons to apply for future climate change scenarios. Journal of Marine Science and Engineering 9, 759.
| Crossref | Google Scholar |

Pachauri RK, Allen MR, Barros VR, Broome J, Cramer W, Christ R, Church JA, Clarke L, Dahe Q, Dasgupta P, Dubash NK, Edenhofer O, Elgizouli I, Field CB, Forster P, Friedlingstein P, Fuglestvedt J, Gomez-Echeverri L, Hallegatte S, Hegerl G, Howden M, Jiang K, Jimenez Cisneros B, Kattsov V, Lee H, Mach KJ, Marotzke J, Mastrandrea MD, Meyer L, Minx J, Mulugetta Y, O’Brien K, Oppenheimer M, Pereira JJ, Pichs-Madruga R, Plattner G-K, Pörtner H-O, Power SB, Preston B, Ravindranath NH, Reisinger A, Riahi K, Rusticucci M, Scholes R, Seyboth K, Sokona Y, Stavins R, Stocker TF, Tschakert P, van Vuuren D, van Ypersele J-P (2014) Climate change 2014, synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. (Intergovernmental Panel on Climate Change: Geneva, Switzerland) Available at https://www.ipcc.ch/site/assets/uploads/2018/02/SYR_AR5_FINAL_full.pdf

Paschke K, Cumillaf JP, Loyola S, Gebauer P, Urbina M, Chimal ME, Pascual C, Rosas C (2010) Effect of dissolved oxygen level on respiratory metabolism, nutritional physiology, and immune condition of southern king crab Lithodes santolla (Molina, 1782) (Decapoda, Lithodidae). Marine Biology 157, 7-18.
| Crossref | Google Scholar |

Peck LS, Culley MB, Helm MM (1987) A laboratory energy budget for the ormer Haliotis tuberculata L. Journal of Experimental Marine Biology and Ecology 106(2), 103-123.
| Crossref | Google Scholar |

Peck LS, Morley SA, Richard J, Clark MS (2014) Acclimation and thermal tolerance in Antarctic marine ectotherms. The Journal of Experimental Biology 217, 16-22.
| Crossref | Google Scholar |

Prince J (2005) Combating the tyranny of scale for Haliotids: micro-management for microstocks. Marine Science 76(2), 557-577 Available at http://researchrepository.murdoch.edu.au/id/eprint/24520.
| Google Scholar |

Ragg NLC, Taylor HH (2006) Oxygen uptake, diffusion limitation, and diffusing capacity of the bipectinate gills of the abalone, Haliotis iris (Mollusca: Prosobranchia). Comparative Biochemistry and Physiology – A. Molecular & Integrative Physiology 143, 299-306.
| Crossref | Google Scholar |

Ragg NLC, Watts E (2015) Physiological indicators of stress and morbidity in commercially handled abalone Haliotis iris. Journal of Shellfish Research 34(2), 455-467.
| Crossref | Google Scholar |

Rogers-Bennett L, Catton CA (2019) Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens. Scientific Reports 9(1), 15050.
| Crossref | Google Scholar |

Rogers-Bennett L, Dondanville RF, Moore JD, Vilchis LI (2010) Response of red abalone reproduction to warm water, starvation, and disease stressors: implications of ocean warming. Journal of Shellfish Research 29(3), 599-611.
| Crossref | Google Scholar |

Rogers-Bennett L, Klamt R, Catton CA (2021) Survivors of climate driven abalone mass mortality exhibit declines in health and reproduction following kelp forest collapse. Frontiers in Marine Science 8, 725134.
| Crossref | Google Scholar |

Sarà G, Romano C, Widdows J, Staff FJ (2008) Effect of salinity and temperature on feeding physiology and scope for growth of an invasive species (Brachidontes pharaonis – MOLLUSCA: BIVALVIA) within the Mediterranean sea. Journal of Experimental Marine Biology and Ecology 363(1–2), 130-136.
| Crossref | Google Scholar |

Sea Temperature Info (2022) Christchurch water temperature by month. Available at https://seatemperature.info/new-zealand/christchurch-water-temperature.html [Verified 28 May 2022]

Searle T, Roberts RD, Lokman PM (2006) Effects of temperature on growth of juvenile blackfoot abalone, Haliotis iris Gmelin. Aquaculture Research 37(14), 1441-1449.
| Crossref | Google Scholar |

Shao Y, Li C, Chen X, Zhang P, Li Y, Li T, Jiang J (2015) Metabolomic responses of sea cucumber Apostichopus japonicus to thermal stresses. Aquaculture 435, 390-397.
| Crossref | Google Scholar |

Shin SR, Kim HJ, Lee DH, Kim H, Sohn YC, Kim JW, Lee JS (2020) Gonadal maturation and main spawning period of Haliotis gigantea (Gastropoda: Haliotidae). Development & Reproduction 24(2), 79-88.
| Crossref | Google Scholar | PubMed |

Somero GN (2012) The physiology of global change: linking patterns to mechanisms. Annual Review of Marine Science 4, 39-61.
| Crossref | Google Scholar | PubMed |

Steinarsson A, Imsland AK (2003) Size dependent variation in optimum growth temperature of red abalone (Haliotis rufescens). Aquaculture 224(1–4), 353-362.
| Crossref | Google Scholar |

Sterman MD, Foster JF (1956) Conformation changes in bovine plasma albumin associated with hydrogen ion and urea binding. I. Intrinsic viscosity and optical rotation 1,2. Journal of the American Chemical Society 78(15), 3652-3656.
| Crossref | Google Scholar |

Stuart MD, Brown MT (1994) Growth and diet of cultivated black-footed abalone, Haliotis iris (Martyn). Aquaculture 127(4), 329-337.
| Crossref | Google Scholar |

Thomsen MS, Mondardini L, Alestra T, Gerrity S, Tait L, South PM, Lilley SA, Schiel DR (2019) Local extinction of bull kelp (Durvillaea spp.) due to a marine heatwave. Frontiers in Marine Science 6, 84.
| Crossref | Google Scholar |

Venter L, Loots DT, Vosloo A, Jansen van Rensburg P, Lindeque JZ (2018) Abalone growth and associated aspects: now from a metabolic perspective. Reviews in Aquaculture 10(2), 451-473.
| Crossref | Google Scholar |

Vilchis LI, Tegner MJ, Moore JD, Friedman CS, Riser KL, Robbins TT, Dayton PK (2005) Ocean warming effects on growth, reproduction, and survivorship of southern California abalone. Ecological Applications 15(2), 469-480.
| Crossref | Google Scholar |

Vinberg GG (1960) ‘Rate of metabolism and food requirements of fishes.’ (Fisheries Research Board of Canada)

Vosloo D, Vosloo A (2010) Response of cold-acclimated, farmed South African abalone (Haliotis midae) to short-term and long-term changes in temperature. Journal of Thermal Biology 35(7), 317-323.
| Crossref | Google Scholar |

Vosloo D, Vosloo A, Morillion EJ, Samuels JN, Sommer P (2013) Metabolic readjustment in juvenile South African abalone (Haliotis midae) acclimated to combinations of temperature and dissolved oxygen levels. Journal of Thermal Biology 38(7), 458-466.
| Crossref | Google Scholar |

Wang Y, Annunziata O (2007) Comparison between Protein-polyethylene Glycol (PEG) interactions and the effect of PEG on protein-protein interactions using the liquid-liquid phase transition. Journal of Physical Chemistry B 111(5), 1222-1230.
| Crossref | Google Scholar | PubMed |

Wells RMG, Baldwin J, Speed SR, Weber RE (1998) Haemocyanin function in the New Zealand abalones Haliotis iris and H. australis: relationships between oxygen-binding properties, muscle metabolism and habitat. Marine and Freshwater Research 49(2), 143-149.
| Crossref | Google Scholar |

Widdows J (1976) Physiological adaptation of Mytilus edulis to cyclic temperatures. Journal of Comparative Physiology 105(2), 115-128.
| Crossref | Google Scholar |

Widdows J, Johnson D (1988) Physiological energetics of Mytilus edulis: scope for growth. Marine Ecology Progress Series 46, 113-121.
| Crossref | Google Scholar |

Yurista PM (1999) Temperature-dependent energy budget of an Arctic Cladoceran, Daphnia middendorffiana. Freshwater Biology 42(1), 21-34.
| Crossref | Google Scholar |

Zhang H, Shin PKS, Cheung SG (2016) Physiological responses and scope for growth in a marine scavenging gastropod, Nassarius festivus (Powys, 1835), are affected by salinity and temperature but not by ocean acidification. ICES Journal of Marine Science 73(3), 814-824.
| Crossref | Google Scholar |