Abstract
The tremendous expansion of Chinese abalone production has not been without challenges such as low salinity stress, which may occur during severe summer rainstorms and typhoon events. Interspecific hybrids have, however, been of great use to the aquaculture industry in withstanding environmental stresses. This study adopted the non-invasive method of measuring heart rate to monitor the cardiac performance of the Pacific abalone and two of its interspecific hybrids during the incidence of continuous salinity decrease. The results showed that low salinity significantly influences the heart rate of abalone. Fluctuation in the abalone’s heartbeat suggests a pattern with three phases and two breakpoints of salinity (BOS1 and BOS2). BOS1 represents an isosmotic point, and BOS2 represents lethal salinity. We argue that relatively lower BOS suggests better tolerance to low salinity, and long-term exposure to salinities around BOS2 could be detrimental to all three species. The hybrid H. discus hannai ♀ x H. fulgens ♂ (DF) recorded the lowest BOS1 and BOS2, which was also significantly different (P = 0.01) from DD at BOS1, suggesting a better tolerance potential for low salinities than the other species. Altogether, our data establish species-specific BOS and reveal the cardiac mechanism by which abalone responds to low salinity. The results confirm that the non-invasive heart rate detection method could likewise be adopted to define critical salinities for abalone, and hybridization could be a potential method to breed the more stress-resilient aquatic animals.
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References
Bakhmet IN, Komendantov AJ, Smurov AO (2012) Effect of salinity change on cardiac activity in Hiatella arctica and Modiolus modiolus, in the White Sea. Polar Biol 35:143–148. https://doi.org/10.1007/s00300-011-1033-y
Boamah GA, Wang T, Chowdhury IA, Luo X, Huang M, Xu C, Ke C, You W (2020) Sub-low salinity impact on survival, growth and meat quality of the Pacific abalone (Haliotis discuss hannai) and hybrids. Aquac Res 51:5184–5193. https://doi.org/10.1111/are.14856
Boarder JS, Maguire GB, Harris JO (2001) Effect of salinity on survival and haemolymph parameters for greenlip abalone. In: Burke et al (eds) Environmental requirements of abalone. University of Tasmania, School of Aquaculture, Launceston, pp 91–97
Burke CM, Harris JO, Hindrum SM, Edwards SJ, Maguire GB (2001) Environmental requirements of abalone. University of Tasmania, School of Aquaculture, Launceston
Calosi P, Chelazzi G, Ugolini A (2003) Optocardiographic recording of heart rate in Talitrus saltator (Amphipoda:Talitridae). Physiol Entomol 28:344–348. https://doi.org/10.1111/j.1365-3032.2003.00348.x
Calosi P, Ugolini A, Morritt D (2005) Physiological responses to hyposmotic stress in supralittoral amphipod Talitrus saltator (Crustacea:Amphipoda). Comp Biochem Physiol A Mol Integr Physiol 142:267–275. https://doi.org/10.1016/j.cbpb.2005.06.012
Casselman MT, Anttila K, Farrell AP (2012) Using maximum heart rate as a rapid screening tool to determine optimum temperature for aerobic scope in Pacific salmon Oncorhynchus spp. J Fish Biol 80:358–377. https://doi.org/10.1111/j.1095-8649.2011.03182.x
Chen JC, Chen WC (2000) Salinity tolerance of Haliotis diversicolor supertexta at different salinity and temperature levels. Aquaculture 181:191–203. https://doi.org/10.1016/S0044-8486(99)00226-4
Chen N, Luo X, Gu Y, Han G, Dong Y, You W, Ke C (2016) Assessment of the thermal tolerance of abalone based on cardiac performance in Haliotis discus hannai, H. gigantean and their interspecific hybrid. Aquaculture 465:258–264. https://doi.org/10.1016/j.aquaculture.2016.09.004
Chen N, Shen Y, Yu F, Luo X, You W, Ke C (2020) A new indicator of hypoxia tolerance in abalone, developed based on heart rate fluctuations. Aquaculture 519:734903. https://doi.org/10.1016/j.aquaculture.2019.734903
Cook PA (2016) Recent trends in worldwide abalone production. J Shellfish Res 5:581–583. https://doi.org/10.2983/035.035.0302
Dong YW, Williams GA (2011) Variations in cardiac performance and heat shock protein expression to thermal stress in two differently zoned limpets on a tropical rocky shore. Mar Biol 158:1223–1231. https://doi.org/10.1007/s00227-011-1642-6
Dubey SK, Trivedi RK, Rout SK, Chand BK, Choudhury A (2014) Median lethal salinity (MLS96 h) of two small indigenous fish species Amblypharyngodon mola and Pethis ticto from Indian Sundarban. J Aquac Res Dev 5:1–6. https://doi.org/10.4172/2155-9546.1000249
Gao X, Li Y, Li X, Wu F, Song C, Liu Y (2017) The response and osmotic pressure regulation mechanism of Haliotis discus hannai (Mollusca, Gastropoda) to sudden salinity changes. Hydrobiologia 797:181–198. https://doi.org/10.1007/s10750-017-3129-z
Ghaffari H, Wang W, Li A, Zhang G, Li L (2019) Thermotolearance divergence revealed by physiological and molecular responses in two oyster subspecies of Crassostrea gigas in China. Front Physiol 10:1137. https://doi.org/10.3389/fphys.2019.011137
Hauton C (2016) Effects of salinity as a stressor to aquatic invertebrates. In: Solan M, Whiteley NM (eds) Stressors in the marine environment, physiological and ecological responses; societal implications. Oxford University Press, Oxford, pp 3–24
Jia Y, Liu X (2018) Expression of Na+/K+-ATPase was affected by salinity change in Pacific abalone Haliotis discus hannai. Front Physiol 9:1–15. https://doi.org/10.3389/fphys.2018.01244
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. Chin J Oceanol Limnol 35:1248–1258. https://doi.org/10.1007/s00343-016-5185-z
Lafarga De La Cruz F, Gallado-Escarate C (2011) Intraspecies and interspecies hybrids in Haliotis: natural and experimental evidence and its impact on abalone aquaculture. Rev Aquac 3:74–99. https://doi.org/10.1111/j.1753-5131.2011.01045.x
Li E, Chen L, Zeng C, Chen X, Yu N, Lai Q, Qin JG (2007) Growth, body composition, respiration and ambient ammonia nitrogen tolerance of juvenile white shrimp, Litopenaeus vannamei, at different salinities. Aquaculture 265:385–390. https://doi.org/10.1016/j.aquaculture.2007.02.018
Liang S, Luo X, You W, Luo L, Ke C (2014) The role of hybridization in improving the immune response and thermal tolerance of abalone. J Fish Shellfish Immunol 39:69–77. https://doi.org/10.1016/j.fsi.2014.04.014
Liang S, Luo X, You W, Ke C (2018) Hybridization improved bacteria resistance in abalone: evidence from physiological and molecular responses. Fish Shellfish Immunol 72:679–689. https://doi.org/10.1016/j.fsi.2017.11.009
Lim HK, Jeong MH, Min BH, Kim SH, Park CJ (2014) Survival rate and oxygen consumption patterns with respect to salinity changes in juvenile abalone Haliotis discus hannai. Anim Cell Syst 18:380–386. https://doi.org/10.1080/19768354.2014.978370
Luo X, Ke C, You W, Wang D (2010) Factors affecting the fertilization success in laboratory hybridization between Haliotis discus hannai and Haliotis gigantea. J Shellfish Res 29:621–625. https://doi.org/10.2983/035.029.0310
Luo X (2009) Study on genetic basis of hybridization between Haliotis sieboldii Reeve and Haliotis discus hannai Ino [D]. Xiamen University (in Chinese with an English abstract)
Manuel AV, Tu PTC, Tsutsui N, Yoshimatsu T (2020) Effect of salinity change and exposure time on egg stages of two abalone species Haliotis discus discus and H. gigantean. Fish Sci 86:27–33. https://doi.org/10.1007/s12562-019-01366-4
Marshall DJ, Dong YW, McQuaid CD, Williams GA (2011) Thermal adaptation in the intertidal snail Echinolittorina malaccana contradicts current theory by revealing the crucial roles of resting metabolism. J Exp Biol 214:3649–3657. https://doi.org/10.1242/jeb.059899
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. Rev Aquac 8:342–368. https://doi.org/10.1111/raq.12097
Nam BH, Park EM, Kim YO, Kim DG, Jee YJ, Lee SJ, An CM (2013) Analysis of heat, cold or salinity stress-inducible genes in the Pacific abalone, Haliotis discus hannai, by suppression substractive hybridization. Korean J Malacology 29:181–187. https://doi.org/10.9710/kjm.2013.29.3.181
Parker LM, Scanes E, O’Connor WA, Coleman RA, Byrne M, Portner HO, Ross PM (2017) Ocean acidification narrows the acute thermal and salinity tolerance of the Sydney rock oyster Saccostrea glomerata. Mar Pollut Bull 122:263–271. https://doi.org/10.1016/j.marpolbul.2017.06.052
Pillai BR, Diwan AD (2002) Effects of acute salinity stress on oxygen consumption and ammonia excretion rates of the marine shrimp Metapenaeus monoceros. J Crustac Biol 22:45–52. https://doi.org/10.1163/20021975-99990207
Portner HO (2010) Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressors effects in marine ecosystems. J Exp Biol 213:881–893. https://doi.org/10.1242/jeb.037523
Rowe CL (2002) Differences in maintenance energy expenditure by two estuarine shrimp (Palaemonetes pugio and P. vulgaris) that may permit partitioning of habitats by salinity. Comp Biochem Physiol A Mol Integr Physiol 132:341–351. https://doi.org/10.1016/S1095-6433(02)00043-0
Sara G, De Pirro M (2011) Heart beat rate adaptations to varying salinity of two intertidal Mediterranean bivalves: the invasive Brachidontes pharaonis and the native Mytilaster minimus. Ital J Zool 78:193–197. https://doi.org/10.1080/11250001003657360
Shen Y, Huang M, You W, Luo X, Ke C (2020) The survival and respiration response of two abalones under short-term hypoxia challenges. Aquaculture 15:735658. https://doi.org/10.1016/j.aquaculture.2020.735658
Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15. https://doi.org/10.1016/j.marenvres.2012.04.003
Stone DAJ, Purvis M, Bansemer MS, Lange B, Schaefer EN, Howarth GS, Harris JO (2014) Dietary intervention improves the survival of culture greenlip abalone (Haliotis laevigata Donovan) at high water temperature. Aquaculture 430:230–240. https://doi.org/10.1016/j.aquaculture.2014.03.047
Ungherese G, Boddi V, Ugolini A (2008) Eco-physiology of Palaemonetes antennarius (Crustacea, Decapoda): the influence of temperature and salinity on cardiac frequency. Physiol Entomol 33:155–161. https://doi.org/10.1111/j.1365-3032.2008.00620.x
Vilas C, Drake P, Pascual E (2006) Oxygen consumption and osmoregulatory capacity in Neomysis integer Reduce competition for resources among mysid shrimp in temperate estuary. Physiol Biochem Zool 79:866–877. https://doi.org/10.1086/506001
Wu F, Zhang G (2016) Pacific abalone farming in China: recent innovations and challenges. J Shellfish Res 35:703–710. https://doi.org/10.2983/035.035.0317
Xing Q, Li Y, Guo H, Yu Q, Huang X, Wang S, Hu X, Zhang L, Bao Z (2016) Cardiac performance: a thermal tolerance indicator in scallops. Mar Biol 163:1–9. https://doi.org/10.1007/s00227-016-3021-9
Yang SJ, Min BH (2019) Sub-optimal or reduction in temperature and salinity decrease antioxidant activity and cellularity in the hemolymph of the Pacific abalone (Haliotis discus hannai). Fish Shellfish Immunol 84:485–490. https://doi.org/10.1016/j.fsi.2018.10.041
You W, Ke CH, Luo X, Wang DX (2009) Growth and survival of three small abalone Haliotis diversicolor populations and their reciprocal crosses. Aquac Res 40:1474–1480. https://doi.org/10.1111/j.1365-2109.2009.02247.x
You W, Guo Q, Fan F, Ren P, Luo X, Ke CH (2015) Experimental hybridization and genetic identification of Pacific abalone Haliotis discus hannai and green abalone H. fulgens. Aquaculture 448:243–249. https://doi.org/10.1016/j.aquaculture.2015.05.043
You W, Wang B, Luo X, Ke CH (2018) Environmental stress tolerance and immune response for the small abalone hybrids. Aquacult Int 27:105–123. https://doi.org/10.1007/s10499-018-0310-y
Zhang P, Dong S, Wang F, Wang H, Gao W, Yan Y (2012) Effect of salinity on growth and energy budget of red and green colour variant sea cucumber Apostichopus japonicas (Selenca). Aquac Res 43:1611–1619. https://doi.org/10.1111/j.1365-2109.2011.02965.x
Funding
This work was supported by the Chinese Government Marine Scholarship (2018SOA015946), the National Key Research and Development Program of China (2018YFD0901401), the National Natural Science Foundation of China (31872564), and the Fujian Provincial S & T Project (2019N0001 and 2020NZ08003).
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Experiment conceptualization and design: Caihuan Ke, Weiwei You, and Grace Afumwaa Boamah. Acquisition of animals, materials, and software for experiment setup and data collection: Xuan Luo, Caihuan Ke, Weiwei You, Feng Yu, and Yawei Shen. Experiment, data collection and analysis, and writing of the first draft manuscript: Grace Afumwaa Boamah. Manuscript revision and preparation of the final draft: Caihuan Ke, Weiwei You, Xuan Luo, Changan Xu, and Grace Afumwaa Boamah.
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All of the methods and animals were approved and performed in agreement with the instructions of the Laboratory Animal Management and Ethics Committee of Xiamen University.
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We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work. There is no professional or other personal interest of any nature or kind in any product, service, or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled, “Fluctuations in the heart rate of abalone in response to low salinity stress.”
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Boamah, G.A., Yu, F., Shen, Y. et al. Fluctuations in the heart rate of abalone in response to low salinity stress. Aquacult Int 30, 173–186 (2022). https://doi.org/10.1007/s10499-021-00790-7
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DOI: https://doi.org/10.1007/s10499-021-00790-7