Rapid recovery of normal gill morphology and blood physiology in brown trout (Salmo trutta) after short-term exposure to toxic concentrations of aqueous aluminium under non-steady state chemical conditions

Submitted: 16 December 2020
Accepted: 14 April 2021
Published: 17 May 2021
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Freshwater acidification is characterised by elevated concentrations of aqueous aluminium. Global emissions of acidifying agents are reduced due to international agreements, and freshwater acidification has shifted from chronic to a more episodic character. The recovery of fish populations in acidified areas is likely to depend on the individual’s ability to recover from short-time aluminium exposures. We exposed brown trout (Salmo trutta) to an Al-rich medium, nominal concentration 600 µg L–1, for 0.5, 2, 6, 8 and 11 hours, before transfer to circumneutral Al-poor water for recovery. As controls, fish were either exposed for 11 hours to an acidified Al-poor medium or to untreated water. Some mortality during the first 24 hours of the recovery period occurred in fish exposed for 11, 8 and 6 hours to aluminium. No mortality during recovery was observed in the remaining groups. Aluminium exposure led to increased haematocrit and plasma lactate concentration, decreased plasma chloride concentration, deposition of aluminium on gill surfaces, and morphological alteration of the gill structures. The responses depended on exposure time. Aluminium deposited on the gill disappeared and plasma lactate levels were at control levels after 1 day in the recovery water, while haematocrit and plasma chloride levels were at control levels after 14 days of recovery. Gills in fish exposed to aluminium for 11 hours were almost fully recovered after 14 days. We conclude that the toxic response in brown trout exposed to an acutely toxic aluminium challenge is reversible. Moreover, the first 24 hours after aluminium exposures is the most critical period for the fish recovery. Further, it takes no more than 14 days for brown trout to fully recover from an acute toxic aluminium exposure, and only 1 day if the aluminium challenge is moderate.



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Alexander AC, Chambers PA, Jeffries DS, 2017. Episodic acidification of 5 rivers in Canada’s oil sands during snowmelt: A 25-year record. Sci. Tot. Environ. 599–600:739–749. DOI: https://doi.org/10.1016/j.scitotenv.2017.04.207
Andersen DO, 2006. Labile aluminium chemistry downstream a limestone treated lake and an acid tributary: effects of warm winters and extreme rainstorms. Sci. Tot. Environ. 366:739–748. DOI: https://doi.org/10.1016/j.scitotenv.2005.09.084
Barnes RB, 1975. The determination of specific forms of aluminum in natural water. Chem. Geol. 15:177–191. DOI: https://doi.org/10.1016/0009-2541(75)90018-2
Cronan CS, Schofield CL, 1979. Aluminium leaching response to acid precipitation: effects on high-elevation watersheds in the northeast. Science 204:304–306. DOI: https://doi.org/10.1126/science.204.4390.304
Denton J, Freemont AJ, Ball J, 1984. Detection and distribution of aluminium in bone. J. Clin. Pathol. 37:136–142. DOI: https://doi.org/10.1136/jcp.37.2.136
Driscoll CT, 1984. A procedure for the fractionation of aqueous aluminum in dilute acidic waters. Intern. J. Environ. Anal. Chem. 16:267–283. DOI: https://doi.org/10.1080/03067318408076957
Driscoll CT, Baker JP, Bisogni JJ, Schofield CL, 1980. Effects of aluminum speciation on fish in dilute acidified waters. Nature 284:161–164. DOI: https://doi.org/10.1038/284161a0
Enge E, Auestad BH, Hesthagen T, 2016. Temporary increase in sea salt deposition accelerates recovery of brown trout (Salmo trutta) populations in very dilute and acidified mountain lakes. Water Air Soil Pollut. 227:208. DOI: https://doi.org/10.1007/s11270-016-2889-9
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. 85:97–177. DOI: https://doi.org/10.1152/physrev.00050.2003
Fakhraei H, Driscoll CT, 2015. Proton and aluminium binding properties of organic acids in surface waters of the Northeastern U.S. Environ. Sci. Technol. 49:2939–2947. DOI: https://doi.org/10.1021/es504024u
Fivelstad S, Leivestad H, 1984. Aluminium toxicity to Atlantic salmon (Salmo salar L.) and brown trout (Salmo trutta L.): mortality and physiological response. Rep. Inst. Freshw. Res. Drottningholm 61:69–77.
Garmo ØA, Skjelkvåle BL, de Wit HA, Colombo L, Curtis C, Fölster J, Hoffmann A, Hruska J, Høgåsen T, Jeffries DS, Keller WB, Kram P, Majer V, Monteith DT, Paterson AM, Rogora M, Rzychon D, Steingruber S, Stoddard JL, Vuorenmaa J, Worsztynowicz A, 2014. Trends in surface water chemistry in acidified areas in Europe and North America from 1990 to 2008. Water Air Soil Pollut. 225:1880. DOI: https://doi.org/10.1007/s11270-014-1880-6
Gensemer RW, Playle RC, 1999. The bioavailability and toxicity of aluminium in aquatic environments. Crit. Rev. Environ. Sci. Technol. 29:315–450. DOI: https://doi.org/10.1080/10643389991259245
Harriman R, Morrison BRS, 1981. Forestry, fisheries and acid rain in Scotland. Scot. Forest. 35:89–95.
Harvey HH, 1975. Fish populations in a large group of acid-stressed lakes. Verh. Int. Ver. Theor. Angew. Limnol. 19:2406–2417. DOI: https://doi.org/10.1080/03680770.1974.11896324
Harwood JE, 1969. The use of an ion-selective electrode for routine fluoride analysis on water samples. Water Res. 3:273–280. DOI: https://doi.org/10.1016/0043-1354(69)90024-4
Hem DJ, Robertson CE. 1976. Form and stability of aluminum hydroxide complexes in dilute solution. Geol Survey Water-suppl Paper 1827-A, U.S. Government Printing Office, Washington DC.
Hesthagen T, Fjellheim A, Schartau AK, Wright RF, Saksgård R, Rosseland BO, 2011. Chemical and biological recovery of Lake Saudlandsvatn, a highly acidified lake in southernmost Norway, in response to decreased acid deposition. Sci. Tot. Environ. 409:2908–2916. DOI: https://doi.org/10.1016/j.scitotenv.2011.04.026
Hesthagen T, Fiske P, Saksgård R, 2016. Recovery of young brown trout (Salmo trutta) in acidified streams: What are the critical values for acid-neutralizing capacity? Atm. Environ. 146:236–244. DOI: https://doi.org/10.1016/j.atmosenv.2016.07.010
Hindar A, Henriksen A, Tørseth K, Semb A, 1994. Acid water and fish death. Nature 372 327–328. DOI: https://doi.org/10.1038/372327b0
Hochachka PW, 1961. The effect of physical training on oxygen debt and glycogen reserves in trout. Can. J. Zool. 39:767–776. DOI: https://doi.org/10.1139/z61-073
Howells G, Dalziel TRK, Reader JP, Solbe JF, 1990. EIFAC water quality criteria for European freshwater fish: report on aluminium. Chem. Ecol. 4:117–173. DOI: https://doi.org/10.1080/02757549008035972
Howells G, Dalziel TRK, Reader JP, Solbe JF, 1994. Aluminium and freshwater fish water quality criteria, p. 55–115. In: G. Howells (ed), Water quality for freshwater fish. Gordon and Breach Sci. Publ., London. DOI: https://doi.org/10.1201/9781482287158
Johannessen M, Skartveit A, Wright RF, 1980. Streamwater chemistry before, during and after snowmelt, p. 224–225. In: D. Drabløs and A. Tollan (eds), Ecological impact of acid precipitation. SNSF project, Ås, Norway.
Kowalik RA, Ormerod SJ, 2006. Intensive sampling and transplantation experiments reveal continued effects of episodic acidification on sensitive stream invertebrates. Freshwater Biol. 51:180–191. DOI: https://doi.org/10.1111/j.1365-2427.2005.01476.x
Kroglund F, Teien HC, Rosseland BO, Salbu B, Lucassen ECHET, 2001. Water quality dependent recovery from aluminium stress in Atlantic salmon smolt. Water Air Soil Pollut. 130:911–916. DOI: https://doi.org/10.1023/A:1013811719192
Kroglund F, Finstad B, Pettersen K, Teien HC, Salbu B, Rosseland BO, Nilsen TO, Stefansson S, Ebbesson LOE, Nilsen R, Bjørn PA, Kristensen T, 2012. Recovery of Atlantic salmon smolts following aluminum exposure defined by changes in blood physiology and seawater tolerance. Aquaculture 362–363:232–240. DOI: https://doi.org/10.1016/j.aquaculture.2011.04.041
Lacroix GL, Peterson RH, Belfry CS, Martin-Robichauda DJ, 1993. Aluminum dynamics on gills of Atlantic salmon fry in the presence of citrate and effects on integrity of gill structure. Aquat. Toxicol. 27:373–401. DOI: https://doi.org/10.1016/0166-445X(93)90065-9
Lappivaara J, Nikinmaa M, Tuurala H, 1995. Arterial oxygen tension and the structure of the secondary lamellae of the gills in rainbow trout (Oncorhynchus mykiss) after acute exposure to zinc and during recovery. Aquat. Toxicol. 32:321–331. DOI: https://doi.org/10.1016/0166-445X(94)00097-A
Laudon H, Bishop KH, 1999. Quantifying sources of acid neutralisation capacity depression during spring flood episodes in northern Sweden. Environ. Pollut. 105:427–435. DOI: https://doi.org/10.1016/S0269-7491(99)00036-6
Lawrence GB, David MB, Lovett GM, Murdoch PS, Burns DA, Stoddard JL, Baldigo BP, Porter JH, Thompson AW, 1999. Soil calcium status and the response of stream chemistry to changing acidic deposition rates. Ecol. Appl. 9:1059–1072. DOI: https://doi.org/10.1890/1051-0761(1999)009[1059:SCSATR]2.0.CO;2
Likens GE, Wright RF, Galloway JN, Butler TJ, 1979. Acid Rain. Sci. Am. 241:43–51. DOI: https://doi.org/10.1038/scientificamerican1079-43
Lydersen E, Poléo ABS, Muniz IP, Salbu B, Bjørnstad HE, 1990. The effects of naturally occurring high and low molecular weight inorganic and organic species on the yolk-sack larvae of Atlantic salmon (Salmo salar L.) exposed to acidic aluminium-rich lake water. Aquat. Toxicol. 18:219–230. DOI: https://doi.org/10.1016/0166-445X(90)90003-8
Lydersen E, Poléo ABS, Nandrup Pettersen M, Riise G, Salbu B, Kroglund F, Rosseland BO, 1994. The importance of in situ measurements to relate toxicity and chemistry in dynamic aluminium freshwater systems. J. Ecol. Chem. 3:357–365.
McWilliams PG, 1980. Acclimation to an acid medium in the brown trout Salmo trutta. J. Exp. Biol. 88:269–280. DOI: https://doi.org/10.1242/jeb.88.1.269
Milligan CL, Wood CM, 1982. Disturbances in haematology, fluid volume distribution and circulatory function associated with low environmental pH in the rainbow trout, Salmo gairdneri. J. Exp. Biol. 99:397–415. DOI: https://doi.org/10.1242/jeb.99.1.397
Mitrovic D, Dymowska A, Nilsson GE, Perry SF, 2009. Physiological consequences of gill remodelling in goldfish (Carassius auratus) during exposure to long-term hypoxia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297:R224–R234. DOI: https://doi.org/10.1152/ajpregu.00189.2009
Mueller ME, Sanchez DA, Bergman HL, McDonald DG, Rhem RG, Wood CM, 1991. Nature and time course of acclimation to aluminium in juvenile brook trout (Salvelinus fontinalis). II. Gill histology. Can. J. Fish. Aquat. Sci. 48:2016–2027. DOI: https://doi.org/10.1139/f91-240
Muniz IP, 1984. The effects of acidification on Scandinavian freshwater fish fauna. Phil. Trans. Royal Soc. London 305: 517–528. DOI: https://doi.org/10.1098/rstb.1984.0074
Muniz IP, Leivestad H, 1980a. Acidification effects on freshwater fish, p. 84–92. In: D. Drabløs and A. Tollan (eds.), Ecological impact of acid precipitation. SNSF project, Ås, Norway.
Muniz IP, Leivestad H, 1980b. Toxic effects of aluminium on the brown trout, Salmo trutta L., p. 320–321. In: D. Drabløs and A. Tollan (eds.), Ecological impact of acid precipitation. SNSF project, Ås, Norway.
Neville CM, 1985. Physiological response of juvenile rainbow trout, Salmo gairdneri, to acid and aluminum – Prediction of field responses from laboratory data. Can. J. Fish. Aquat. Sci. 42:2004–2019. DOI: https://doi.org/10.1139/f85-248
Nilsen TO, Ebbesson LOE, Handeland SO, Kroglund F, Finstad B, Angotzi AR, Stefansson SO, 2013. Atlantic salmon (Salmo salar L.) smolts require more than two weeks to recover from acidic water and aluminium exposure. Aquat. Toxicol. 142–142:33–44. DOI: https://doi.org/10.1016/j.aquatox.2013.07.016
Nilsson GE, Dymowska A, Stecyk JAW, 2012. New insights into the plasticity of gill structure. Resp. Physiol. Neurobiol. 184:214–222. DOI: https://doi.org/10.1016/j.resp.2012.07.012
Norrgren L, Wicklund GA, Malmborg O, 1991. Accumulation and effects of aluminium in the minnow (Phoxinus phoxinus L.) at different pH levels. J. Fish Biol. 39:833–847. DOI: https://doi.org/10.1111/j.1095-8649.1991.tb04413.x
Perry SF, Laurent P, 1993. Environmental effects on fish gill structure and function, p. 231–264. In: J.C. Rankin and F.B. Jensen (eds.), Fish ecophysiology. Chapman and Hall, London. DOI: https://doi.org/10.1007/978-94-011-2304-4_9
Plambech M, Van Deurs M, Steffensen JF, Tirsgaard B, Behrens JW, 2013. Excess post-hypoxic oxygen consumption in Atlantic cod Gadus morhua. J. Fish. Biol. 83:396-403. DOI: https://doi.org/10.1111/jfb.12171
Playle RC, Goss GG, Wood CM, 1989. Physiological disturbances in rainbow trout (Salmo gairdneri) during acid and aluminum exposure in soft water of two calcium concentrations. Can. J. Zool. 67:314–324. DOI: https://doi.org/10.1139/z89-046
Poléo ABS, 1995. Aluminium polymerization – a mechanism of acute toxicity of aqueous aluminium to fish. Aquat. Toxicol. 31:347–356. DOI: https://doi.org/10.1016/0166-445X(94)00083-3
Poléo ABS, Bjerkely F, 2000. Effect of unstable aluminium chemistry on Arctic char (Salvelinus alpinus). Can. J. Fisher. Aquat. Sci. 57:1423–1433. DOI: https://doi.org/10.1139/f00-084
Poléo ABS, Hytterød S, 2003. The effect of aluminium in Atlantic salmon (Salmo salar) with special emphasis on alkiline water. J. Inorg. Chem. 97:89–96. DOI: https://doi.org/10.1016/S0162-0134(03)00261-7
Poléo ABS, Lydersen E, Muniz IP, 1991. The influence of temperature on aqueous aluminium chemistry and survival of Atlantic salmon (Salmo salar L.) fingerlings. Aquat. Toxicol. 21:267–278. DOI: https://doi.org/10.1016/0166-445X(91)90077-M
Poléo ABS, Lydersen E, Rosseland BO, Kroglund F, Salbu B, Vogt RD, Kvellestad A, 1994. Increased mortality of fish due to changing Al-chemistry of mixing zones between limed streams and acidic tributaries. Water Air Soil Pollut. 75:339–351. DOI: https://doi.org/10.1007/BF00482945
Poléo ABS, Muniz IP, 1993. The effect of aluminium in soft water at low pH and different temperatures on mortality, ventilation frequency and water balance in smoltifying Antlantic salmon (Salmo salar L.). Environ. Biol. Fish. 36:193–203. DOI: https://doi.org/10.1007/BF00002799
Poléo ABS, Øxnevad SA, Østbye K, Andersen RA, Oughton DH, Vøllestad LA, 1995. Survival of crucian carp, Carassius carassius, exposed to a high low-molecular weight inorganic aluminium challenge. Aquat. Sci. 57:350–359. DOI: https://doi.org/10.1007/BF00878398
Poléo ABS, Østbye K, Øxnevad SA, Andersen RA, Heibo E, Vøllestad LA, 1997. Toxicity of acid aluminium-rich water to seven freshwater fish species: a comparative laboratory study. Environ. Pollut. 96: 129–139. DOI: https://doi.org/10.1016/S0269-7491(97)00033-X
Poléo ABS, Schjolden J, Sørensen J, Nilsson GE, 2017. The high tolerance to aluminium in crucian carp (Carassius carassius) is associated with its ability to avoid hypoxia. PLoS One 12:e0179519. DOI: https://doi.org/10.1371/journal.pone.0179519
Pye MC, Vaughan IP, Ormerod SJ, 2012. Episodic acidification affects the breakdown and invertebrate colonisation of oak litter. Freswater Biol. 57:2318–2329. DOI: https://doi.org/10.1111/fwb.12007
Rask M, Mannio J, Forsius M, Posch M, Vuorinen PJ, 1995. How many fish populations in Finland are affected by acid precipitation? Environ. Biol. Fish. 42:51–63. DOI: https://doi.org/10.1007/BF00002351
Rosseland BO, Blakar IA, Bulger A, Kroglund F, Kvellestad A, Lydersen E, Oughton DH, Salbu B, Staurnes M, Vogt R, 1992. The mixing zone between limed and acidic river waters: Complex aluminium chemistry and extreme toxicity for salmonids. Environ. Pollut. 78:3–8. DOI: https://doi.org/10.1016/0269-7491(92)90003-S
Schjolden J, Sørensen J, Nilsson GE, Poléo ABS, 2007. The toxicity of copper to crucian carp (Carassius carassius) in soft water. Sci. Total Environ. 384:239–251. DOI: https://doi.org/10.1016/j.scitotenv.2007.06.009
Schofield CL, 1976. Acid precipitation. Effects on fish. Ambio 5:5–6.
Seip HM, Andersen DO, Christophersen N, Sullivan TJ, Vogt RD, 1989. Variations in concentrations of aqueous aluminium and other chemical species during hydrological episodes at Birkenes, southernmost Norway. J. Hydrol. 108:387–405. DOI: https://doi.org/10.1016/0022-1694(89)90295-3
Serrano I, Buffam I, Palm D, Brannas E, Laudon H, 2008. Thresholds for survival of brown trout during the spring flood acid pulse in streams high in dissolved organic carbon. Trans. Am. Fish. Soc. 137:1363–1377. DOI: https://doi.org/10.1577/T07-069.1
Skartveit A, Gjessing YT, 1979. Chemical budgets and chemical quality of snow and runoff during spring snowmelt. Nordic Hydrol. 10:141–154. DOI: https://doi.org/10.2166/nh.1979.0018
Skjelkvåle BL, Wright RF, Henriksen A, 1998. Norwegian lakes show widespread recovery from acidification: results of national surveys of lake water chemistry 1986–1997. Hydrol. Earth Syst. Sci. 2:555–562. DOI: https://doi.org/10.5194/hess-2-555-1998
Skjelkvåle BL, Wilander A, Hindar A, Borg H, 2007. Large scale patterns of chemical recovery in lakes in Norway and Sweden: importance of sea salt episodes and changes in dissolved organic carbon. Appl. Geochem. 22:1174–1180. DOI: https://doi.org/10.1016/j.apgeochem.2007.03.040
Sparling DW, Lowe TP, 1996. Environmental hazards of aluminum to plants, invertebrates, fish, and wildlife. Rev. Environ. Contam. Toxicol. 145:1–127. DOI: https://doi.org/10.1007/978-1-4612-2354-2_1
Staurnes M, Sigholt T, Reite OB, 1984. Reduced carbonic anhydrase and Na-K-ATPase activity in gills of salmonids exposed to aluminium-containing acid water. Experientia 40:226–227. DOI: https://doi.org/10.1007/BF01963613
Stoddard JL, Jeffries DS, Lükewille A, Clair TA, Dillon PJ, Driscoll CT, Forsius M, Johannessen M, Kahl JS, Kellogg JH, Kemp J, Mannio J, Monteith DT, Murdoch PS, Patrick S, Rebsdorf A, Skjelkvåle BL, Stainton MP, Traaen T, van Dam H, Webster KE, Wieting J, Wilander A, 1999. Regional trends in aquatic recovery from acidification in North America and Europe. Nature 401:575–578. DOI: https://doi.org/10.1038/44114
Svendsen JC, Steffensen JF, Aarestrup K, Frisk M, Etzerodt A, Jyde M, 2012. Excess posthypoxic oxygen consumption in rainbow trout (Oncorhynchus mykiss): recovery in normoxia and hypoxia. Can. J. Zool. 90:1–11. DOI: https://doi.org/10.1139/z11-095
Vuorinen M, Vuorinen PJ, Peuranen S, 1993. Lethal and sublethal threshold values of aluminium and acidity to pike (Esox Lucius), whitefish (Coregonus lavaretus pallasi), pike perch (Stizostedion lucioperca) and roach (Rutilus rutilus) yolk-sac fry. Sci. Tot. Environ. 134:s953–967. DOI: https://doi.org/10.1016/S0048-9697(05)80102-0
Weatherley NS, Rutt GP, Thomas P, Ormerod SJ, 1991. Liming acid streams: aluminium toxicity to fish in mixing zones. Water Air Soil Pollut. 55:345–353. DOI: https://doi.org/10.1007/BF00211199
Wellington BI, Driscoll CT, 2004. The episodic acidification of a stream with elevated concentrations of dissolved organic carbon. Hydrol. Processes 18:2663–2680. DOI: https://doi.org/10.1002/hyp.5574
Wigington PJ, Davies TD, Tranter M, Eshleman KN, 1992. Comparison of episodic acidification in Canada, Europe and the United States. Environ. Pollut. 78:29–35. DOI: https://doi.org/10.1016/0269-7491(92)90006-V
Wigington PJ, DeWalle DR, Murdoch PS, Kretser WA, Simonin HA, Van Sickle J, Baker JP, 1996. Episodic acidification of small streams in the northeastern United States: ionic controls of episodes. Ecol. Appl. 6:389–407. DOI: https://doi.org/10.2307/2269378
Wilkinson KJ, Campbell PGC, 1993. Aluminum bioconcentration at the gill surface of juvenile Atlantic salmon in acidic media. Environ. Toxicol. Chem. 12:2083–2095. DOI: https://doi.org/10.1002/etc.5620121116
Witters HE, 1986. Acute acid exposure of rainbow trout, Salmo gairdneri Richardson: effects of aluminium and calcium on ion balance and haematology. Aquat. Toxicol. 8:197–210. DOI: https://doi.org/10.1016/0166-445X(86)90065-2
Wright RF, 2008. The decreasing importance of acidification episodes with recovery from acidification: an analysis of the 30-year record from Birkenes, Norway. Hydrol. Earth Syst. Sci. 12:353–362. DOI: https://doi.org/10.5194/hess-12-353-2008
Wright RF, Snekvik E, 1978. Acid precipitation: chemistry and fish population in 700 lakes in southernmost Norway. Verh. Intern. Ver. Theor. Angew. Limnol. 20:765–775. DOI: https://doi.org/10.1080/03680770.1977.11896597

Edited by

Franz Hoelker, Leibniz Institute of Freshwater Ecology and Inland Fisheries, Berlin, Germany

How to Cite

Poléo, Antonio Bjørn Stefano, Birgitte Marie Kjelsberg, Nina Alstad Rukke, and Leif Asbjørn Vøllestad. 2021. “Rapid Recovery of Normal Gill Morphology and Blood Physiology in Brown Trout (<em>Salmo trutta</Em>) After Short-Term Exposure to Toxic Concentrations of Aqueous Aluminium under Non-Steady State Chemical Conditions”. Journal of Limnology 80 (2). https://doi.org/10.4081/jlimnol.2021.2000.