Abstract
Acute stress response in the European bitterling, Rhodeus amarus, to glochidia parasitism by the invasive unionid mussel, Sinanodonta woodiana, was quantified by analysing cortisol plasma levels using liquid chromatography coupled to mass spectrometer. We tested a novel method which required as little as 4 µL of plasma by increasing the volume using charcoal-treated plasma. Bitterling were observed to increase cortisol levels significantly in response to glochidia infestation. Overall, this technique allows the precise measurement of steroid hormone plasma concentrations in small fish.
Data availability
The original data and the R code for data analyses are available in FigShare repository (https://doi.org/10.6084/m9.figshare.20805766).
References
Benkő-Kiss Á, Ferincz Á, Kováts N, Paulovits G (2013) Spread and distribution pattern of Sinanodonta woodiana in Lake Balaton. Knowl Manag Aquat Ecosyst 408:09. https://doi.org/10.1051/kmae/2013043
Chowdhury MMR, Marjomäki TJ, Taskinen J (2021) Effect of glochidia infection on growth of fish: freshwater pearl mussel Margaritifera margaritifera and brown trout Salmo trutta. Hydrobiologia 848:3179–3189. https://doi.org/10.1007/s10750-019-03994-4
Douda K, Vrtílek M, Slavík O, Reichard M (2012) The role of host specificity in explaining the invasion success of the freshwater mussel Anodonta woodiana in Europe. Biol Invasions 14:127–137. https://doi.org/10.1007/s10530-011-9989-7
Douda K, Liu H-Z, Yu D, Rouchet R, Liu F, Tang Q-I, Methling C, Smith C, Reichard M (2017) The role of local adaptation in shaping fish-mussel coevolution. Freshw Biol 62:1858–1868. https://doi.org/10.1111/fwb.13026
Douda K, Velíšek J, Kolářová J, Rylková K, Slavík O, Horký P, Langrová I (2017) Direct impact of invasive bivalve (Sinanodonta woodiana) parasitism on freshwater fish physiology: evidence and implications. Biol Invasions 19:989–999. https://doi.org/10.1007/s10530-016-1319-7
Douda K, Martin M, Glidewell E, Barnhart C (2018) Stress-induced variation in host susceptibility to parasitic freshwater mussel larvae. Hydrobiologia 810:265–272. https://doi.org/10.1007/s10750-016-2895-3
Dubansky B, Whitaker B, Galvez F (2011) Influence of cortisol on the attachment and metamorphosis of larval Utterbackia imbecillis on bluegill sunfish (Lepomis macrochirus). Biol Bull 220:97–106. https://doi.org/10.1086/BBLv220n2p97
Gorityala S, Yang S, Montano MM, Xu Y (2018) Simultaneous determination of dihydrotestosterone and its metabolites in mouse sera by LC-MS/MS with chemical derivatization. J Chromatogr b: Anal Technol Biomed Life Sci 1090:22–35. https://doi.org/10.1016/j.jchromb.2018.05.008
Higashi T, Nishio T, Hayashi N, Shimada K (2007) Alternative procedure for charged derivatization to enhance detection responses of steroids in electrospray ionization-MS. Chem Pharm Bull 55:662–665. https://doi.org/10.1248/cpb.55.662
Howerth EW, Keller AE (2006) Experimentally induced glochidiosis in smallmouth bass (Micropterus dolomieu). Vet Pathol 43:1004–1007. https://doi.org/10.1354/vp.43-6-1004
Isorna E, de Pedro N, Valenciano AI, Alonso-Gómez ÁL, Delgado MJ (2017) Interplay between the endocrine and circadian systems in fishes. J Endocrinol 232(3):R141–R159. https://doi.org/10.1530/JOE-16-0330
Konečný A, Popa OP, Bartáková V, Douda K, Bryja J, Smith C, Popa LO (2018) Modelling the invasion history of Sinanodonta woodiana in Europe: tracking the routes of a sedentary aquatic invader with mobile parasitic larvae. Evol Appl 11:1975–1989. https://doi.org/10.1111/eva.12700
Methling C, Douda K, Reichard M (2019) Intensity-dependent energetic costs in a reciprocal parasitic relationship. Oecologia 191:285–294. https://doi.org/10.1007/s00442-019-04504-y
Modesto V, Ilarri M, Souza AT, Lopes-Lima M, Douda K, Clavero M, Sousa R (2018) Fish and mussels: importance of fish for freshwater mussel conservation. Fish Fish 19:244–259. https://doi.org/10.1111/faf.12252
Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268. https://doi.org/10.1023/A:1008924418720
Reichard M, Ondračková M, Przybylski M, Liu H, Smith C (2006) The costs and benefits in an unusual symbiosis: experimental evidence that bitterling fish (Rhodeus sericeus) are parasites of unionid mussels in Europe. J Evol Biol 19:788–796. https://doi.org/10.1111/j.1420-9101.2005.01051.x
Reichard M, Vrtílek M, Douda K, Smith C (2012) An invasive species reverses the roles in a host–parasite relationship between bitterling fish and unionid mussels. Biol Lett 8:601–604. https://doi.org/10.1098/rsbl.2011.1234
Rigby MC, Hechinger RF, Stevens L (2002) Why should parasite resistance be costly? Trends Parasitol 18:116–120. https://doi.org/10.1016/S1471-4922(01)02203-6
Rock SL, Watz J, Nilsson PA, Österling M (2022) Effects of parasitic freshwater mussels on their host fishes: a review. Parasitology. https://doi.org/10.1017/S0031182022001226
Sadoul B, Geffroy B (2019) Measuring cortisol, the major stress hormone in fishes. J Fish Biol 94:540–555. https://doi.org/10.1111/jfb.13904
Sánchez-Vázquez FJ, López-Olmeda JF, Vera LM, Migaud H, López-Patiño MA, Míguez JM (2019) Environmental cycles, melatonin, and circadian control of stress response in fish. Front Endocrinol 10:279. https://doi.org/10.3389/fendo.2019.00279
Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321. https://doi.org/10.1016/0169-5347(96)10039-2
Slavík O, Horký P, Douda K, Velíšek J, Kolářová J, Lepič P (2017) Parasite-induced increases in the energy costs of movement of host freshwater fish. Physiol Behav 171:127–134. https://doi.org/10.1016/j.physbeh.2017.01.010
Smith C, Reichard M, Jurajda P, Przybylski M (2004) The reproductive ecology of the European bitterling (Rhodeus sericeus). J Zool 262:107–124. https://doi.org/10.1017/S0952836903004497
Taeubert JE, Geist J (2013) Critical swimming speed of brown trout (Salmo trutta) infested with freshwater pearl mussel (Margaritifera margaritifera) glochidia and implications for artificial breeding of an endangered mussel species. Parasitol Res 112:1607–1613. https://doi.org/10.1007/s00436-013-3314-6
Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625. https://doi.org/10.1152/physrev.1997.77.3.591
Acknowledgements
We thank two referees for their constructive comments on the manuscript and Rowena Spence for comments and English corrections. Cortisol quantification was performed in Karel Harant Laboratory of mass spectrometry and OMICS analysis at BIOCEV Research Center, Faculty of Science, Charles University.
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Funding came from the Czech Science Foundation project (19-05510S) to K.D.
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MR conceived and designed the study, analysed the data and wrote the manuscript, KD performed experimental infestations, RB collected blood samples, and AB analysed cortisol levels. All authors revised and approved the final version of the manuscript.
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The care and use of experimental animals complied with Czech and EU animal welfare laws, guidelines and policies as approved by ethical committee of the Ministry of Education (MSMT 18809/2019–5, individual licence: CZ01285).
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The authors declare no competing interests.
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Reichard, M., Douda, K., Blažek, R. et al. Increased plasma cortisol level as acute response to glochidia parasitism. Environ Biol Fish 106, 101–106 (2023). https://doi.org/10.1007/s10641-022-01379-6
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DOI: https://doi.org/10.1007/s10641-022-01379-6