Abstract
Magnolia denudata is a well-known ornamental tree in China due to its beautiful blossoms, and it has been used as an analgesic to treat human headaches. This study investigated the anesthetic potential and physiological response of the essential oil of M. denudata flowers on spotted seabass Lateolabrax maculatus. Fish (mean ± SD, 164.16 ± 15.40 g) were individually exposed to different concentrations of M. denudata essential oil (MDO, 10, 20, 40, 60, 80, 100, and 120 mg/L) and eugenol (10, 20, 30, 40, 50, 60, and 70 mg/L) to investigate anesthetic efficacy. Based on the ideal time criterion for anesthetic induction (< 3 min) and recovery (< 10 min), the lowest effective concentration for spotted seabass was 100 mg/L for MDO and 60 mg/L for eugenol. The physiological and histopathological damage in the gill of L. maculatus after using MDO and eugenol was also evaluated at the minimum dose inducing deep anesthesia, and at 0, 6, and 24 h after recovery. The results showed that MDO and eugenol anesthesia alleviated the levels of cortisol and glucose and the lactic dehydrogenase activity induced by handling. Compared with eugenol, MDO also caused secondary stress to the body, but MDO caused minor physiological responses and histological changes in the gills. This study suggests that MDO is an effective anesthetic for spotted seabass.
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References
Afifi SH, Al-Thobaiti S, Rasem BM (2000) Multiple exposure of Asian sea bass, (Lates calcarifer, Centropomidae) to clove oil: a histopathological study. Ass Vet Med J 42(84):166–174
Ainsworth AJ, Bowser PR, Beleau MH (1985) Serum cortisol levels in channel catfish, from production ponds. Prog Fish-Cult 47(3):176–181. https://doi.org/10.1577/1548-8640(1985)47<176:SCLICC>2.0.CO;2
Aydın B, Barbas L (2020) Sedative and anesthetic properties of essential oils and their active compounds in fish: a review. Aquaculture 520:734999. https://doi.org/10.1016/j.aquaculture.2020.734999
Aydın İ, Akbulut B, Küçük E, Kumlu M (2015) Effects of temperature, fish size and dosage of clove oil on anesthesia in turbot (Psetta maxima Linnaeus, 1758). Turk J Fish Aquat Sc 15(4):899–904. https://doi.org/10.4194/1303-2712-v15_4_13
Bahrekazemi M, Yousefi N (2017) Plasma enzymatic, biochemical and hormonal responses to clove oil, 2-phenoxy ethanol, and MS-222 exposed to Caspian brown trout (Salmo trutta caspius, kessleri). Iran J Aquat Anim Health 3(1):47–60. https://doi.org/10.18869/acadpub.ijaah.3.1.47
Baptista-Silva S, Borges S, Ramos OL, Pintado M, Sarmento B (2020) The progress of essential oils as potential therapeutic agents: A review. J Essent Oil Res 32(4):279–295. https://doi.org/10.1080/10412905.2020.1746698
Barata M, Soares F, Aragão C, Almeida AC, Pousão-Ferreira P, Ribeiro L (2016) Efficiency of 2-phenoxyethanol and clove oil for reducing handling stress in reared meagre, Argyrosomus regius (Pisces: Sciaenidae). J World Aquacult Soc 47:82–92. https://doi.org/10.1111/jwas.12245
Boaventura TP, Souza CF, Ferreira AL, Favero GC, Baldissera MD, Heinzmann BM, Baldisserotto B, Luz RK (2020) Essential oil of Ocimum gratissimum (Linnaeus, 1753) as anesthetic for Lophiosilurus alexandri: induction, recovery, hematology, biochemistry and oxidative stress. Aquaculture 529:735676. https://doi.org/10.1016/j.aquaculture.2020.735676
Bodur T, León-Bernabeu S, Navarro A, Tort L, Afonso JM, Montero D (2018) Effects of new plant based anesthetics Origanum sp. and Eucalyptus sp. oils on stress and welfare parameters in Dicentrarchus labrax and their comparison with clove oil. Aquaculture 495:402–408. https://doi.org/10.1016/j.aquaculture.2018.06.021
Boonen B, Alpizar YA, Benoy V, Van Den Bosch L, Voets T, Talavera K (2014) The Trpa1 agonist cinnamaldehyde acts as a local anesthetic inhibiting voltage-gated sodium channels in sensory neurons. Biophys J 106(2):326a–327a. https://doi.org/10.1016/j.bpj.2013.11.1879
Brandão FR, Farias CFS, de Melo Souza DC, de Oliveira MIB, de Matos LV, Majolo C, de Oliveira MR, Chaves FCM, de Almeida O’Sullivan FL, Chagas EC (2021) Anesthetic potential of the essential oils of Aloysia triphylla, Lippia sidoides and Mentha piperita for Colossoma macropomum. Aquaculture 534:736275. https://doi.org/10.1016/j.aquaculture.2020.736275
Cao X, Wang Y, Yu N, Le Q, Hu J, Yang Y, Kuang S, Zhang M, Sun Y, Gu W, Yan X (2019) Transcriptome analysis reveals the influence of anaesthetic stress on the immune system of crucian carp (Carassius auratus) under the process of treatment and low concentration transport by MS-222 and Eugenol. Aquac Res 50(11):3138–3153. https://doi.org/10.1111/are.14268
Carter KM, Woodley CM, Brown RS (2011) A review of tricaine methanesulfonate for anesthesia of fish. Rev Fish Biol Fisher 21(1):51–59. https://doi.org/10.1007/s11160-010-9188-0
Cheng CH, Guo ZX, Luo SW, Wang AL (2018) Effects of high temperature on biochemical parameters, oxidative stress, DNA damage and apoptosis of pufferfish (Takifugu obscurus). Ecotoxicol Environ Saf 150:190–198. https://doi.org/10.1016/j.ecoenv.2017.12.045
Cifuentes-Rius A, Desai A, Yuen D, Johnston AP, Voelcker NH (2021) Inducing immune tolerance with dendritic cell-targeting nanomedicines. Nat Nanotechnol 16(1):37–46. https://doi.org/10.1126/science.1122545
de Lima CL, Morales-Gamba RD, Malcher Neto TS, Barcellos JFM, Heinzmann BM, Schmidt D, Baldisserotto B, Marcon JL (2021) Eugenol and Lippia alba essential oils as effective anesthetics for the Amazonian freshwater stingray Potamotrygon wallacei (Chondrichthyes, Potamotrygonidae). Fish Physiol Biochem 1–20. https://doi.org/10.1007/s10695-021-01029-1
Dong H, Wang W, Duan Y, Li H, Liu Q, Sun Y, Zhang J (2020a) Transcriptomic analysis of juvenile Chinese sea bass (Lateolabrax maculatus) anesthetized by MS-222 (tricaine methanesulfonate) and eugenol. Fish Physiol Biochem 1–12.https://doi.org/10.1007/s10695-019-00755-x
Dong H, Sun Y, Duan Y, Li H, Li Y, Liu Q, Wang W, Zhang J (2020b) The effect of teprenone on the intestinal morphology and microbial community of Chinese sea bass (Lateolabrax maculatus) under intermittent hypoxic stress. Fish Physiol Biochem 46(5):1873–1882
dos Santos Batista E, Brandão FR, Majolo C, Inoue LAKA, Maciel PO, de Oliveira MR, Chaves FCM, Chagas EC (2018) Lippia alba essential oil as anesthetic for tambaqui. Aquaculture 495:545–549. https://doi.org/10.1016/j.aquaculture.2018.06.040
dos Santos Teixeira N, Marques LS, Rodrigues RB, Gusso D, Pinheiro GT, Machado TLF, Streit DP Jr (2021) Effects of anesthetic MS-222 on stress and reproduction of South American silver catfish (Rhamdia quelen) males. Anim Reprod Sci 225:106669. https://doi.org/10.1016/j.anireprosci.2020.106669
Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85(1):97–177. https://doi.org/10.1152/physrev.00050.2003
Fazio F (2019) Fish hematology analysis as an important tool of aquaculture: a review. Aquaculture 500:237–242. https://doi.org/10.1016/j.aquaculture.2018.10.030
Ferreira JT, Schoonbee HJ, Smit GL (1984) The uptake of the anaesthetic benzocaine hydrochloride by the gills and the skin of three freshwater fish species. J Fish Biol 25(1):35–41. https://doi.org/10.1111/j.1095-8649.1984.tb04848.x
Galano A, Alvarez-Idaboy JR (2011) Glutathione: mechanism and kinetics of its non-enzymatic defense action against free radicals. RSC Adv 1(9):1763–1771. https://doi.org/10.1039/C1RA00474C
Ghayyur S, Khan MF, Tabassum S, Ahmad MS, Sajid M, Badshah K, Muhammad AK, Saira Ghayyur S, Khan NK, Ahmad B, Qamer S (2021) A comparative study on the effects of selected pesticides on hemato-biochemistry and tissue histology of freshwater fish Cirrhinus mrigala (Hamilton, 1822). Saudi J Biol Sci 28(1):603-611
Hanggono B (2006) Application of clove oil as anesthetic for sea bass (Lates calcarifer Bloch) Jurnal Perikanan. J Fish Sci VIII(1):9–16
Haschek WM, Rousseaux CG, Wallig MA (2009) Fundamentals of Toxicologic Pathology. Academic Press, San Diego
He R, Lei B, Su Y, Wang A, Cui K, Shi X, Chen X (2020) Effectiveness of eugenol as an anesthetic for adult spotted sea bass (Lateolabrax maculatus). Aquaculture 523:735180. https://doi.org/10.1016/j.aquaculture.2020.735180
Hoseini SM, Rajabiesterabadi H, Kordrostami S (2016) Chronic exposure of Rutilus rutilus caspicus fingerlings to ambient copper: effects on food intake, growth performance, biochemistry and stress resistance. Toxicol Ind Health 32(2):375–383. https://doi.org/10.1177/0748233713500825
Hunn JB, Allen JL (1974) Movement of drugs across the gills of fishes. Annu Rev Pharmacol 14(1):47–54. https://doi.org/10.1146/annurev.pa.14.040174.000403
Jerez-Cepa I, Fernández-Castro M, Alameda-López M, González-Manzano G, Mancera JM, Ruiz-Jarabo I (2021) Transport and recovery of gilthead seabream (Sparus aurata L.) sedated with AQUI-S® and etomidate: effects on intermediary metabolism and osmoregulation. Aquaculture. 530:735745. https://doi.org/10.1016/j.aquaculture.2020.735745
Jiao W, Han Q, Xu Y, Jiang H, Xing H, Teng X (2019) Impaired immune function and structural integrity in the gills of common carp (Cyprinus carpio L.) caused by chlorpyrifos exposure: through oxidative stress and apoptosis. Fish Shellfish Immunol 86:239–245. https://doi.org/10.1016/j.fsi.2018.08.060
Junior GB, de Abreu MS, da Rosa JGDS, Pinheiro CG, Heinzmann BM, Caron BO, Baldisserotto B, Barcellos LJG (2018) Lippia alba and Aloysia triphylla essential oils are anxiolytic without inducing aversiveness in fish. Aquaculture 482:49–56. https://doi.org/10.1016/j.aquaculture.2017.09.023
Liang T, Xu X, Ye D, Chen W, Gao B, Huang Y (2019) Caspase/AIF/apoptosis pathway: a new target of puerarin for diabetes mellitus therapy. Mol Biol Rep 46(5):4787–4797. https://doi.org/10.1007/s11033-019-04925-1
Liu XL, Xi QY, Yang L, Li HY, Jiang QY, Shu G, Wang S, Gao P, Zhu XT, Zhang YL (2011) The effect of dietary Panax ginseng polysaccharide extract on the immune responses in white shrimp, Litopenaeus vannamei. Fish Shellfish Immunol 30(2):495–500. https://doi.org/10.1016/j.fsi.2010.11.018
Lu B, Li M, Yin R (2016) Phytochemical content, health benefits, and toxicology of common edible flowers: a review (2000–2015). Crit Rev Food Sci Nutr 56(sup1):S130–S148. https://doi.org/10.1080/10408398.2015.1078276
Maniya NH, Srivastava DN (2020) Fabrication of porous silicon based label-free optical biosensor for heat shock protein 70 detection. Mater Sci Semicond Process 115:105126. https://doi.org/10.1016/j.mssp.2020.105126
Martínez-Porchas M, Martínez-Córdova LR, Ramos-Enriquez R (2009) Cortisol and glucose: reliable indicators of fish stress? Pan-Am J Aquat Sci 158–178. https://www.scopus.com/inward/record.uri?partnerID=HzOxMe3b&scp=68349148307&origin=inward
Martos-Sitcha JA, Wunderink YS, Straatjes J, Skrzynska AK, Mancera JM, Martínez-Rodríguez G (2014) Different stressors induce differential responses of the CRH-stress system in the gilthead sea bream (Sparus aurata). Comp Biochem Physiol Part A: Mol Integr Physiol 177:49–61. https://doi.org/10.1016/j.cbpa.2014.07.021
Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fisher 9(3):211–268. https://doi.org/10.1023/A:1008924418720
Netto JDL, Oliveira RSM, Copatti CE (2017) Efficiency of essential oils of Ocimum basilicum and Cymbopogum flexuosus in the sedation and anaesthesia of Nile tilapia juveniles. An Acad Bras Cienc 89:2971–2974. https://doi.org/10.1590/0001-3765201720170001
Ouyang MY, Wen B, Ma HC, Chen C, Gao JZ, Zhang Y, Chen ZZ (2020) Minimally invasive evaluation of the anaesthetic efficacy of MS-222 for ornamental discus fish using skin mucus biomarkers. Aquac Res 51(7):2926–2935. https://doi.org/10.1111/are.14631
Park CH, Park SY, Lee SY, Kim JK, Park SU (2018) Analysis of metabolites in white flowers of Magnolia denudata Desr. and violet flowers of Magnolia liliiflora Desr. Molecules 23(7):1558. https://doi.org/10.3390/molecules23071558
Purbosari N, Warsiki E, Syamsu K, Santoso J (2019) Natural versus synthetic anesthetic for transport of live fish: a review. Aquacult Fish 4(4):129–133. https://doi.org/10.1016/j.aaf.2019.03.002
Purbosari N, Warsiki E, Syamsu K, Santoso J, Effendi I (2021) Evaluation of the application of seaweed (Eucheuma cottonii) extract as fish anesthetic agent. Aquacult Int 1–16.https://doi.org/10.1007/s10499-021-00693-7
Readman GD, Owen SF, Murrell JC, Knowles TG (2013) Do fish perceive anaesthetics as aversive? PLoS One 8:e73773. https://doi.org/10.1371/journal.pone.0073773
Roche H, Bogé G (1996) Fish blood parameters as a potential tool for identification of stress caused by environmental factors and chemical intoxication. Mar Environ Res 41(1):27–43. https://doi.org/10.1016/0141-1136(95)00015-1
Ross LG, Ross B (2009) Anaesthetic and sedative techniques for aquatic animals. Wiley
Saccol EM, Toni C, Pês TS, Ourique GM, Gressler LT, Silva LV, Mourão R, Oliveira R, Baldisserotto B, Pavanato MA (2017) Anaesthetic and antioxidant effects of Myrcia sylvatica (G. Mey.) DC. and Curcuma longa L. essential oils on tambaqui (Colossoma macropomum). Aquacult Res 48(5):2012–2031. https://doi.org/10.1111/are.13034
Saccol EM, Jerez-Cepa I, Ourique GM, Pês TS, Gressler LT, Mourão RH, Martínez-Rodríguezd G, Mancerab JM, Baldisserottoa B, Pavanato MA, Martos-Sitcha JA (2018) Myrcia sylvatica essential oil mitigates molecular, biochemical and physiological alterations in Rhamdia quelen under different stress events associated to transport. Res Vet Sci 117:150–160. https://doi.org/10.1016/j.rvsc.2017.12.009
Schreck CB, Tort L (2016) The concept of stress in fish. In: Fish physiology (vol 35, pp 1–34). Academic Press. https://doi.org/10.1016/B978-0-12-802728-8.00001-1
Semenkova TB, Bayunova LV, Boev AA, Dyubin VP (1999) Effects of stress on serum cortisol levels of sturgeon in aquaculture. J Appl Ichthyol 15(4–5):270–272. https://doi.org/10.1111/j.1439-0426.1999.tb00249.x
Silva LDL, Garlet QI, Koakoski G, Abreu MSD, Mallmann CA, Baldisserotto B, Barcellos LG, Heinzmann BM (2015) Anesthetic activity of the essential oil of Ocimum americanum in Rhamdia quelen (Quoy & Gaimard, 1824) and its effects on stress parameters. Neotrop Ichthyol 13:715–722. https://doi.org/10.1590/1982-0224-20150012
Skår MW, Haugland GT, Powell MD, Wergeland HI, Samuelsen OB (2017) Development of anaesthetic protocols for lumpfish (Cyclopterus lumpus L.): effect of anaesthetic concentrations, sea water temperature and body weight. PloS One 12(7):e0179344. https://doi.org/10.1371/journal.pone.0179344
Souza CDF, Baldissera MD, Salbego J, Lopes JM, Vaucher RDA, Mourão RHV, Caron BO, Heinzmann BM, da Silva LFV, Baldisserotto B (2017) Physiological responses of Rhamdia quelen (Siluriformes: Heptapteridae) to anesthesia with essential oils from two different chemotypes of Lippia alba. Neotrop Ichthyol 15. https://doi.org/10.1590/1982-0224-20160083
Sun Y, Dong H, Zhan A, Wang W, Duan Y, Xie M, Liu Q, Li H, Zhang J (2020) Protection of teprenone against hypoxia and reoxygenation stress in stomach and intestine of Lateolabrax maculatus. Fish Physiol Biochem 46(2):575–584. https://doi.org/10.1007/s10695-019-00732-4
Taheri Mirghaed A, Ghelichpour M, Zargari A, Yousefi M (2018) Anaesthetic efficacy and biochemical effects of 1, 8-cineole in rainbow trout (Oncorhynchus mykiss, Walbaum, 1792). Aquac Res 49(6):2156–2165. https://doi.org/10.1111/are.13671
Teixeira RR, de Souza RC, Sena AC, Baldisserotto B, Heinzmann BM, Couto RD, Copatti CE (2017) Essential oil of Aloysia triphylla in Nile tilapia: anaesthesia, stress parameters and sensory evaluation of fillets. Aquac Res 48(7):3383–3392. https://doi.org/10.1111/are.13165
Toni C, Becker AG, Simões LN, Pinheiro CG, de Lima Silva L, Heinzmann BM, Caron B, O., Baldisserotto, B. (2014) Fish anesthesia: effects of the essential oils of Hesperozygis ringens and Lippia alba on the biochemistry and physiology of silver catfish (Rhamdia quelen). Fish Physiol Biochem 40(3):701–714. https://doi.org/10.1007/s10695-013-9877-4l
Toni C, Martos-Sitcha JA, Baldisserotto B, Heinzmann BM, de Lima Silva L, Martínez-Rodríguez G, Mancera JM (2015) Sedative effect of 2-phenoxyethanol and essential oil of Lippia alba on stress response in gilthead sea bream (Sparus aurata). Res Vet Sci 103:20–27. https://doi.org/10.1016/j.rvsc.2015.09.006
Wang R, Jia H, Wang J, Zhang Z (2010) Flowering and pollination patterns of Magnolia denudata with emphasis on anatomical changes in ovule and seed development. Flora-Morphol Distrib Funct Ecol Plants 205(4):259–265. https://doi.org/10.1016/j.flora.2009.04.003
Wang W, Dong H, Sun Y, Cao M, Duan Y, Li H, Liu Q, Gu Q, Zhang J (2019) The efficacy of eugenol and tricaine methanesulphonate as anaesthetics for juvenile Chinese sea bass (Lateolabrax maculatus) during simulated transport. J Appl Ichthyol 35(2):551–557. https://doi.org/10.1111/jai.13844
Wang W, Dong H, Sun Y, Sun C, Duan Y, Gu Q, Li Y, Xie M, Zhang J (2020) Immune and physiological responses of juvenile Chinese sea bass (Lateolabrax maculatus) to eugenol and tricaine methanesulfonate (MS-222) in gills. Aquacult Rep 18:100554. https://doi.org/10.1016/j.aqrep.2020.100554
Yokogawa K, Seki S (1995) Morphological and genetic differences between Japanese and Chinese sea bass of the genus Lateolabrax. Jpn J Ichthyol 41(4):437–445. https://doi.org/10.11369/jji1950.41.437
Yousefi M, Hoseini SM, Vatnikov YA, Nikishov AA, Kulikov EV (2018) Thymol as a new anesthetic in common carp (Cyprinus carpio): efficacy and physiological effects in comparison with eugenol. Aquaculture 495:376–383. https://doi.org/10.1016/j.aquaculture.2018.06.022
Yousefi M, Vatnikov YA, Kulikov EV, Ghelichpour M (2019) Change in blood stress and antioxidant markers and hydromineral balance of common carp (Cyprinus carpio) anaesthetized with citronellal and linalool: comparison with eugenol. Aquacult Res 50(4):1313–1320. https://doi.org/10.1111/are.14007
Zahl IH, Samuelsen O, Kiessling A (2012) Anaesthesia of farmed fish: implications for welfare. Fish Physiol Biochem 38(1):201–218. https://doi.org/10.1007/s10695-011-9565-1
Zhang T, Yan Z, Zheng X, Wang S, Fan J, Liu Z (2020) Effects of acute ammonia toxicity on oxidative stress, DNA damage and apoptosis in digestive gland and gill of Asian clam (Corbicula fluminea). Fish Shellfish Immunol 99:514–525. https://doi.org/10.1016/j.fsi.2019.11.056
Zhang J, Wu M, Zhang M, Chen X, Yang J (2021) Analysis on aroma components of flowers of five Magnolia denudata cultivars. IOP Conf Ser: Earth Environ Sci 705(1):012007. IOP Publishing
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This research was supported by the fun of Key-Area Research and Development Program of Guangdong Province (2021B0202030001), China—ASEAN Maritime Cooperation Fund Project “China—ASEAN Modern Marine Fishery Technical Cooperation and Industrial Development Demonstration,” the fund of Central Public-interest Scientific Institution Basal Research Fund, South China Sea Fisheries Research Institute, CAFS (2021SD19), the fund of Guangdong Province Modern Agricultural Industrial Technology System Innovation Team Building Project (2022KJ150), the fund of Guangzhou Science and Technology Planning Project (201904010169), the fund of National Key Research and Development Plan Projects (2019YFD0900500), and the fund of Guangdong Province Supporting Town and Villages Technology Commissioner Project (KTP20210259).
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X.Z., H.D. and J.Z. designed the experiment. X.Z. and H.D. performed the experiments, data analyses, and drafted the manuscript.W.J., W.W., Y.D. and J.C. contributed with essential materials. All authors have given approval to the final version of the manuscript, decided to submit the work for publication. The authors like to thank all the laboratory members for experimental material preparation and technical assistance, and thank to Prof. Jian Qin, Flinders University, for providing revisions and suggestions in the manuscript writing.
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Zeng, X., Dong, H., Wu, J. et al. Essential oil of Magnolia denudata is an effective anesthetic for spotted seabass (Lateolabrax maculatus): a test of its effect on blood biochemistry, physiology, and gill morphology. Fish Physiol Biochem 48, 1349–1363 (2022). https://doi.org/10.1007/s10695-022-01124-x
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DOI: https://doi.org/10.1007/s10695-022-01124-x