Experimental observations on ultrastructure of scales of red seabream (Pagrosomus major) for seawater pH monitoring

Hou, Weili; Tian, Li; Sun, Xin; Li, Xin; Chen, Xiangming; Song, Haijun

doi:10.26881/oahs-2025.1.29

Abstract

Ocean acidification monitoring relies predominantly on field test and numerical modeling, while bioindicators are emerging as practical and economic approaches for seawater pH monitoring. Here, we report indoor dissolution experiments on the scale of red seabream (Pagrosomus major) under varied pH (from 7.1 to 7.9), showing that the mean aspect ratio of ventral ctenii and caudal/ventral lepidonts negatively correlated with pH. We propose to employ these ultrastructures of fish scale to be a novel bioindicator for marine pH reconstruction. This semiquantitative proxy would be applicable to both contemporary biomonitoring and paleo-oceanic pH reconstruction for the extensive occurrences of fish in modern oceans and fossil records.

References

Abdullah, H. Z., Idris, M. I., Te Chuan, L., Dermawan, S. K., & Jaffri, M. Z. (2023). Natural hydroxyapatite from black tilapia fish bones and scales for biomedical applications. In: Wan Kamarul Zaman, W. S. & Nurul, A. A. (eds), Sustainable Material for Biomedical Engineering Application. Singapore: Springer Nature Singapore, 107-124. https://doi.org/10.1007/978-981-99-2267-3_6
Search in Google Scholar Back to article
Alkaladi, A., Harabawy, A. S., & Mekkawy, I. A. (2013). Scale characteristics of two fish species, Acanthopagrus bifasciatus (Forsskål, 1775) and Rhabdosargus sarba (Forsskål, 1775) from the Red Sea at Jeddah, Saudi Arabia. Pakistan Journal of Biological Sciences: PJBS, 16(8), 362–371. https://doi.org/10.3923/pjbs.2013.362.371
Search in Google Scholar Back to article
Alves, A. L., Marques, A. L., Martins, E., Silva, T. H., & Reis, R. L. (2017). Cosmetic potential of marine fish skin collagen. Cosmetics, 4(4), 39. https://doi.org/10.3390/cosmetics4040039
Search in Google Scholar Back to article
Antczak, M., & Bodzioch, A. (2018). Diversity of fish scales in Late Triassic deposits of Krasiejów (SW Poland). Paleontological Research, 22(1), 91–100. https://doi.org/10.2517/2017PR012
Search in Google Scholar Back to article
Bergstad, O. A. (1991). Distribution and trophic ecology of some gadoid fish of the Norwegian deep: 2. Food-web linkages and comparisons of diets and distributions. Sarsia, 75(4), 315–325. https://doi.org/10.1080/00364827.1991.10413456
Search in Google Scholar Back to article
Bielajew, B. J., Hu, J. C., & Athanasiou, K. A. (2020). Collagen: Quantification, biomechanics and role of minor subtypes in cartilage. Nature Reviews Materials, 5(10), 730–747. https://doi.org/10.1038/s41578-020-0213-1
Search in Google Scholar Back to article
Cai, L., Wu, X., Dong, Z., Li, X., Yi, S., & Li, J. (2014). Physicochemical responses and quality changes of red sea bream (Pagrosomus major) to gum arabic coating enriched with ergothioneine treatment during refrigerated storage. Food Chemistry, 160(2014), 82–89. https://doi.org/10.1016/j.foodchem.2014.03.093
Search in Google Scholar Back to article
Caldeira, K., & Wickett, M. E. (2003). Anthropogenic carbon and ocean pH. Nature, 425(6956), 365–365. https://doi.org/10.1038/425365a
Search in Google Scholar Back to article
Caldeira, K., & Wickett, M. E. (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. Journal of Geophysical Research, 110, 1–12. https://doi.org/10.1029/2004JC002671
Search in Google Scholar Back to article
Cooley, S. R., & Doney, S. C. (2009). Anticipating ocean acidification’s economic consequences for commercial fisheries. Environmental Research Letters, 4(2), 024007. https://doi.org/10.1088/1748-9326/4/2/024007
Search in Google Scholar Back to article
Cui, X., Friedman, M., Yu, Y., Zhu, Y. A., & Zhu, M. (2023). Bony-fish-like scales in a Silurian maxillate placoderm. Nature Communications, 14(1), 7622. https://doi.org/10.1038/s41467-023-43557-9
Search in Google Scholar Back to article
Damodaran, S. & Parkin, K. L. (2017). Amino acids, peptides, and proteins. In: Damodaran, S., Parkin, K. L. & Fennema, O. R. (eds), Fennema’s food chemistry. Boca Raton: CRC Press, 235–356.
Search in Google Scholar Back to article
Doney, S. C., Fabry, V. J., Feely, R. A., & Kleypas, J. A. (2009). Ocean acidification: The other CO₂ problem. Annual Review of Marine Science, 1(1), 169–192. https://doi.org/10.1146/annurev.marine.010908.163834
Search in Google Scholar Back to article
Echreshavi, S., Al Jufaili, S. M., & Esmaeili, H. R. (2023). Imaging scale surface topography of an endemic cyprinid fish, Garra sharq from the Arabian Peninsula: An integrated optical light and scanning electron microscopy approach. Acta Zoologica, 104(4), 657–676. https://doi.org/10.1111/azo.12449
Search in Google Scholar Back to article
Esmaeili, H. R., Zarei, F., Sanjarani Vahed, N., & Masoudi, M. (2019). Scale morphology and phylogenetic character mapping of scale-surface microstructures in sixteen Aphanius species (Teleostei: Aphaniidae). Micron, 119(2019), 39–53. https://doi.org/10.1016/j.micron.2019.01.002
Search in Google Scholar Back to article
Feely, R. A., Alin, S. R., Newton, J., Sabine, C. L., Warner, M., Devol, A., Krembs, C., & Maloy, C. (2010). The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuarine, Coastal and Shelf Science, 88(4), 442–449. https://doi.org/10.1016/j.ecss.2010.05.004
Search in Google Scholar Back to article
Feely, R. A., Doney, S. C., & Cooley, S. R. (2009). Ocean acidification: Present conditions and future changes in a high-CO₂ world. Oceanography, 22(4), 36–47. https://www.jstor.org/stable/24861022. https://doi.org/10.5670/oceanog.2009.95
Search in Google Scholar Back to article
Foster, W. J., Hirtz, J. A., Farrell, C., Reistroffer, M., Twitchett, R. J., & Martindale, R. C. (2022). Bioindicators of severe ocean acidification are absent from the end-Permian mass extinction. Scientific Reports, 12(1), 1202. https://doi.org/10.1038/s41598-022-04991-9
Search in Google Scholar Back to article
Fouda, M. M. (1979). Studies on scale structure in the common goby Pomatoschistus microps Krøyer. Journal of Fish Biology, 15(2), 173–183. https://doi.org/10.1111/j.1095-8649.1979. tb03581.x
Search in Google Scholar Back to article
Frimodt, C. (1995). Multilingual illustrated guide to the world’s commercial coldwater fish (pp. xix+–244). Oxford.
Search in Google Scholar Back to article
Fu, J., Chen, C., & Chu, Y. (2019). Spatial–temporal variations of oceanographic parameters in the Zhoushan sea area of the East China Sea based on remote sensing datasets. Regional Studies in Marine Science, 28(2019), 100626. https://doi.org/10.1016/j.rsma. 2019.100626
Search in Google Scholar Back to article
Gattuso, J. P., & Hansson, L. (Eds.). (2011). Ocean acidification. Oxford University Press.
Search in Google Scholar Back to article
Gaylord, B., Rivest, E., Hill, T., Sanford, E., Shukla, P., Ninokawa, A., & Ng, G. (2018). California mussels as bio-indicators of ocean acidification. California’s Fourth Climate Change Assessment.
Search in Google Scholar Back to article
Gil-Díaz, T., Haroun, R., Tuya, F., Betancor, S., & Viera-Rodriguez, M. A. (2014). Effects of ocean acidification on the brown alga Padina pavonica: Decalcification due to acute and chronic events. Plos One, 9(9), e108630. https://doi.org/10.1371/journal.pone.0108630
Search in Google Scholar Back to article
Hamm, R. (1986). Functional properties of the myofibrillar system and their measurements. In (P. J. Bechtel Ed.). Muscle as food. Food Science and Technology (pp. 135–191). Academic Press Inc. https://doi.org/10.1016/B978-0-12-084190-5.50009-6
Search in Google Scholar Back to article
Harabawy, A. S. A. (2002). Biological and taxonomic studies on some fish species of the genus Lethrinus (Family: Lethrinidae) from the Red Sea, Egypt and the genus Abramis (Family: Cyprinidae) from the Baltic drainage [Doctoral dissertation, Ph.D. Thesis, Assiut University, Egypt].
Search in Google Scholar Back to article
Harabawy, A. S., Mekkawy, I. A., & Alkaladi, A. (2012). Identification of three fish species of genus Plectorhynchus from the Red Sea by their scale characteristics. Life Science Journal, 9(4), 4472–4485. https://doi.org/10.7537/marslsj090412.673
Search in Google Scholar Back to article
Hutchinson, J. J., & Trueman, C. N. (2006). Stable isotope analyses of collagen in fish scales: Limitations set by scale architecture. Journal of Fish Biology, 69(6), 1874–1880. https://doi.org/10.1111/j.1095-8649.2006.01234.x
Search in Google Scholar Back to article
Ibáñez, A. L., & Jawad, L. A. (2018). Morphometric variation of fish scales among some species of rattail fish from New Zealand waters. Journal of the Marine Biological Association of the United Kingdom, 98(8), 1991–1998. https://doi.org/10.1017/S0025315418000024
Search in Google Scholar Back to article
Iglesias-Rodriguez, M. D. (2012). Ocean acidification. In: Orcutt, J. (ed.), Earth system monitoring: Selected entries from the encyclopedia of sustainability science and technology. Berlin: Springer, 269–289. https://doi.org/10.1007/978-1-4614-5684-1_12
Search in Google Scholar Back to article
Kaur, R., & Dua, A. (2012). Fish scales as indicators of wastewater toxicity from an international water channel Tung Dhab drain. Environmental Monitoring and Assessment, 184(5), 2729–2740. https://doi.org/10.1007/s10661-011-2147-y
Search in Google Scholar Back to article
Kaur, K., Kaur, R., & Kaur, A. (2016). Surface microstructural features of scales in relation to toxic stress of Basic Violet-1. Environmental Science and Pollution Research International, 23(2), 1173–1182. https://doi.org/10.1007/s11356-015-5374-x
Search in Google Scholar Back to article
Khanna, D. R., Sarkar, P., Gautam, A., & Bhutiani, R. (2007). Fish scales as bio-indicator of water quality of River Ganga. Environmental Monitoring and Assessment, 134(1–3), 153–160. https://doi.org/10.1007/s10661-007-9606-5
Search in Google Scholar Back to article
Lanzing, W. J. R., & Higginbotham, D. R. (1974). Scanning microscopy of surface structures of Tilapia mossambica (Peters) scales. Journal of Fish Biology, 6(3), 307–310. https://doi.org/10.1111/j.1095-8649.1974.tb04547.x
Search in Google Scholar Back to article
Lippitsch, E. (1993). A phyletic study on lacustrine haplochromine fishes (Perciformes, Cichlidae) of East Africa, based on scale and squamation characters. Journal of Fish Biology, 42(6), 903–946. https://doi.org/10.1111/j.1095-8649.1993.tb00399.x
Search in Google Scholar Back to article
Liu, W. T., & Xie, X. (2017). Space observation of carbon dioxide partial pressure at ocean surface. IEEE Journal of Selected Topics in Applied Earth Observations and Remote Sensing, 10(12), 5472–5484. https://doi.org/10.1109/JSTARS.2017.2766138
Search in Google Scholar Back to article
Li, D., Wang, B., Jin, H., Miao, Y., Sun, Q., Lin, H., Li, H., Liu, Q., Zhou, F., & Chen, J. (2024). Decoupling of high-resolution surface pH and DO reveals temporal algal bloom dynamics on the East China Sea. Water Research, 261(2024), 122030. https://doi.org/10.1016/j. watres. 2024.122030
Search in Google Scholar Back to article
Marshall, D. J., Abdelhady, A. A., Wah, D. T. T., Mustapha, N., Gödeke, S. H., De Silva, L. C., & Hall-Spencer, J. M. (2019). Biomonitoring acidification using marine gastropods. Science of the Total Environment, 692(2019), 833–843. https://doi.org/10.1016/j. scitotenv. 2019.07.041
Search in Google Scholar Back to article
Mekkawy, I.A.A., Mahmoud, U.M., & Harabawy, A.S.A. (2003). Identification of four Labeo fish species from the Nile, Egypt by their scale characteristics and scanning electron microscopy. Journal of Union of Arab Biologists Cairo. A, Zoology, 19(A):81-104.
Search in Google Scholar Back to article
Mekkawy, I.A.A., Shehata, S.M.A., Saber, S.A. and Osman, A.G.M. (1999). Scale characteristics of five species of genus Epinephelus (Family: Serranidae) from the Red Sea Egypt. Journal-Egyptian German Society of Zoology, 30(B): 71–102.
Search in Google Scholar Back to article
Meyer, F.W., Cardini, U., Wild, C. (2015). Ocean Acidification and Related Indicators. In: Armon, R., Hänninen, O. (eds) Environmental Indicators. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9499-2_41
Search in Google Scholar Back to article
Miller, M. R., Oakes, R. L., Covert, P. A., Ianson, D., & Dower, J. F. (2023). Evidence for an effective defense against ocean acidification in the key bioindicator pteropod Limacina helicina. ICES Journal of Marine Science, 80(5), 1329–1341. https://doi.org/10.1093/icesjms/fsad059
Search in Google Scholar Back to article
Ní Longphuirt, S., Stengal, D., O’dowd, C., & McGovern, E. (2010). Ocean acidification: An emerging threat to our marine environment. Marine Institute.
Search in Google Scholar Back to article
NOAA. (2025). Ocean acidification. National Oceanic and Atmospheric Administration. https://www.noaa.gov/education/resource-collections/ocean-coasts/ocean-acidification
Search in Google Scholar Back to article
Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R. M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R. G., Plattner, G. K., Rodgers, K. B., … Yool, A. (2005). Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature, 437(7059), 681–686. https://doi.org/10.1038/nature04095
Search in Google Scholar Back to article
Pal, G. K., & Suresh, P. V. (2017). Comparative assessment of physico-chemical characteristics and fibril formation capacity of thermostable carp scales collagen. Materials Science and Engineering: C, 70(Pt–1), 32–40. https://doi.org/10.1016/j.msec.2016.08.047
Search in Google Scholar Back to article
Pulikkottil Rajan, D. (2024). Derivatives of Structural Proteins. In: Raman, M., Sasidharan, A., Sabu, S. & Pulikkottil Rajan, D. (eds), Fish structural proteins and its derivatives: Functionality and applications. Singapore: Springer Nature Singapore, 73–105.
Search in Google Scholar Back to article
Renjith, R. K., Jaiswar, A. K., Chakraborty, S. K., Jahageerdar, S., & Sreekanth, G. B. (2014). Application of scale shape variation in fish systematics-an illustration using six species of the family Nemipteridae (Teleostei: Perciformes). Indian Journal of Fisheries, 61(1), 88–92. https://doi.org/10.21077/
Search in Google Scholar Back to article
Ridgwell, A., & Schmidt, D. N. (2010). Past constraints on the vulnerability of marine calcifiers to massive carbon dioxide release. Nature Geoscience, 3(3), 196–200. https://doi.org/10.1038/ngeo755
Search in Google Scholar Back to article
Rishi, K. K., & Jain, M. (1998). Effect of toxicity of cadmium on scale morphology in Cyprinus carpio (Cyprinidae). Bulletin of Environmental Contamination and Toxicology, 60(2), 323–328. https://doi.org/10.1007/s001289900629
Search in Google Scholar Back to article
Sabine, C. L., Feely, R. A., Gruber, N., Key, R. M., Lee, K., Bullister, J. L., Wanninkhof, R., Wong, C. S., Wallace, D. W. R., Tilbrook, B., Millero, F. J., Peng, T.-H., Kozyr, A., Ono, T., & Rios, A. F. (2004). The oceanic sink for anthropogenic CO₂. Science, 305(5682), 367–371. https://doi.org/10.1126/science.1097403
Search in Google Scholar Back to article
Sarker, S. A., Satoh, S., & Kiron, V. (2005). Supplementation of citric acid and amino acid-chelated trace element to develop environment-friendly feed for red sea bream, Pagrus major. Aquaculture, 248(1–4), 3–11. https://doi.org/10.1016/j.aquaculture.2005.04.012
Search in Google Scholar Back to article
Shackleton, L. Y. (1987). A comparative study of fossil fish scales from three upwelling regions. South African Journal of Marine Science, 5(1), 79–84. https://doi.org/10.2989/025776187784522270
Search in Google Scholar Back to article
Silverman, J., Lazar, B., Cao, L., Caldeira, K., & Erez, J. (2009). Coral reefs may start dissolving when atmospheric CO₂ doubles. Geophysical Research Letters, 36,1-5(2009). https://doi.org/10.1029/2008GL036282
Search in Google Scholar Back to article
Solomon S, Qin D, Manning M. Technical summary. In: Solomon S, Qin D, Manning M, Marquis M, Averyt K, Tignor MMB, Miller HL, Chen ZL, editors. Climate change 2007. The physical science basis. Contribution of working group i to the fourth assessment report of the intergovernmental panel on climate change. United Kingdom and New York, NY, USA: Cambridge University Press, Cambridge; 2007. p. 19–91.
Search in Google Scholar Back to article
Tignor, & H. L. Miller (Eds.), Climate change 2007: The physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change.
Search in Google Scholar Back to article
Sutton, T. T. (2013). Vertical ecology of the pelagic ocean: Classical patterns and new perspectives. Journal of Fish Biology, 83(6), 1508–1527. https://doi.org/10.1111/jfb.12263
Search in Google Scholar Back to article
Vasanth, K., Kishore, R. K., Sugumaran, V., Krishnamoorthy, R., Ramdas, R., & Tadepalli, S. K. (2025). Multi-variate hybrid modeling for pacific ocean acidification: predicting future pH trends and analyzing key biogeochemical drivers. CSI Transactions on ICT, 13(1), 99-116. https://doi.org/10.1007/s40012-024-00406-4 11
Search in Google Scholar Back to article
Wainwright, D. K. & Lauder, G. V. 2018. Mucus matters: the slippery and complex surfaces of fish. In: Gorb, S. N. & Gorb, E. V. (eds), Functional Surfaces in Biology III: Diversity of the Physical Phenomena. Cham: Springer International Publishing, 223-246. https://doi.org/10.1007/978-3-319-74144-4_10
Search in Google Scholar Back to article
Wang, Q., Bai, P., Yang, J., Li, P., Yu, C., Wu, Q., Ruan, Z., & Li, B. (2025). Seafloor temperature variability in the Zhoushan Archipelago: Patterns and mechanisms. Estuarine, Coastal and Shelf Science, 320, 109298. https://doi.org/10.1016/j. ecss.2025.109298
Search in Google Scholar Back to article
Weiner, S., & Wagner, H. D. (1998). The material bone: Structure-mechanical function relations. Annual Review of Materials Science, 28(1), 271–298. https://doi.org/10.1146/annurev. matsci.28.1.271
Search in Google Scholar Back to article
Xiao, T., Feng, J., Qiu, Z., Tang, R., Zhao, A., Wong, K., Tsou, J. Y., & Zhang, Y. (2024). Remote-sensing estimation of upwelling-frequent areas in the adjacent waters of Zhoushan (China). Journal of Marine Science and Engineering, 12(7), 1085. https://doi.org/10.3390/jmse12071085
Search in Google Scholar Back to article
Zeebe, R. E., Zachos, J. C., Caldeira, K., & Tyrrell, T. (2008). Carbon emissions and acidification. Science, 321(5885), 51–52. https://doi.org/10.1126/science.1159124
Search in Google Scholar Back to article
Zylberberg, L. (1988). Ultrastructural data on the scales of the dipnoan Protoptems annectens (Sarcopterygii, Osteichthyes). Journal of Zoology, 216(1), 55–71. https://doi.org/10.1111/j.1469-7998.1988.tb02415.x
Search in Google Scholar Back to article
Zylberberg, L. (2004). New data on bone matrix and its proteins. Comptes Rendus Palevol, 3(6–7), 591–604. https://doi.org/10.1016/j.crpv.2004.07.012
Search in Google Scholar Back to article
Zylberberg, L., & Nicolas, G. (1982). Ultrastructure of scales in a teleost (Carassius auratus L.) after use of rapid freeze-fixation and freeze-substitution. Cell and Tissue Research, 223(2), 349–367. https://doi.org/10.1007/BF01258495
Search in Google Scholar Back to article

Experimental observations on ultrastructure of scales of red seabream (Pagrosomus major) for seawater pH monitoring

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