Abstract
The Nuuk harbor is the largest industrial port in Greenland. It is polluted by a number of contaminants including tributyltin (TBT), polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs). Here we analyzed melanomacrophage center (MMC) responses in the spleen and kidney of shorthorn sculpins (Myoxocephalus scorpius) from the harbor and three reference sites in Nuuk, West Greenland. The number and area of splenic MMCs in fish from the most polluted station were significantly lower than those from the less polluted stations (p < 0.01). This suggests that the immune response differed between the fish from the contaminated site and those from the reference sites. This indicates that splenic MMCs of shorthorn sculpins could have a biomarker potential for pollutant exposure. This was, however, not the case for renal MMCs. In addition, this study showed that there were effects of body size on the splenic and renal MMC responses. Therefore, in future studies, body size of shorthorn sculpins needs to be considered when investigating splenic and renal MMC responses.
Similar content being viewed by others
References
Agius C, Roberts RJ (2003) Melano-macrophage centres and their role in fish pathology. J Fish Dis 26:499–509
Antizar-Ladislao B (2008) Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment. A review. Environ Int 34:292–308
Au DWT (2004) The application of histo-cytopathological biomarkers in marine pollution monitoring: a review. Mar Pollut Bull 48:817–834
Barker DE, Khan RA, Lee EM et al (1994) Anomalies in sculpins (Myoxocephalus spp.) sampled near a pulp and paper mill. Arch Environ Contam Toxicol 26:491–496. https://doi.org/10.1007/BF00214152
Basilone G, Gargano A, Corriero A et al (2018) Liver melanomacrophage centres and CYP1A expression as response biomarkers to environmental pollution in European anchovy (Engraulis encrasicolus) from the western Mediterranean Sea. Mar Pollut Bull 131:197–204. https://doi.org/10.1016/j.marpolbul.2018.04.028
Bayoumy EM, Abou-El-dobal SKA, Hassanain MA (2015) Assessment of heavy metal pollution and fish parasites as biological indicators at Arabian gulf off Dammam coast, Saudi Arabia. Int J Zool Res 11:198–206
Bermúdez R, Vigliano F, Marcaccini A et al (2006) Response of Ig-positive cells to Enteromyxum scophthalmi (Myxozoa) experimental infection in turbot, Scophthalmus maximus (L.): A histopathological and immunohistochemical study. Fish Shellfish Immunol 21:501–512. https://doi.org/10.1016/j.fsi.2006.02.006
Bilbao E, Raingeard D, de Cerio OD et al (2010) Effects of exposure to restige-like heavy fuel oil and to perfluorooctane sulfonate on conventional biomarkers and target gene transcription in the thicklip grey mullet Chelon labrosus. Aquat Toxicol 98:282–296. https://doi.org/10.1016/j.aquatox.2010.02.018
Bols NC, Brubacher JL, Ganassin RC, Lee LEJ (2001) Ecotoxicology and innate immunity in fish. Dev Comp Immunol 25:853–873
Carreras-Colom E, Constenla M, Dallarés S, et al (2017) Melanomacrophage centres across seasons, depths and species in the Mediterranean sea: a complex relationship. In: 18th International Conference on Diseases of Fish and Shellfish, p 13508
Cusine DJ, Grant JP (2019) The impact of marine pollution. In: Routledge Library Editions: Pollution, Climate and Change, 1st edn. Routledge. ISBN 9780367358785, p 318
Da Cuña RH, Rey Vázquez G, Piol MN et al (2011) Assessment of the acute toxicity of the organochlorine pesticide endosulfan in Cichlasoma dimerus (Teleostei, Perciformes). Ecotoxicol Environ Saf 74:1065–1073. https://doi.org/10.1016/j.ecoenv.2011.02.002
Dane H, Turgay S (2014) Histopathological changes in gill and liver of Capoeta capoeta living in the Karasu River, Erzurum. Environ Toxicol 30:904–917. https://doi.org/10.1002/tox
Dang M, Basson L, Bach L et al (2019a) Trichodinid infections in internal organs of shorthorn sculpin (Myoxocephalus scorpius) collected around an industrial harbour in Nuuk, Greenland. Parasitology 146:506–510. https://doi.org/10.1017/S0031182018001774
Dang M, Nowell C, Nguyen T et al (2019b) Characterisation and 3D structure of melanomacrophage centers in shorthorn sculpins (Myoxocephalus scorpius). Tissue Cell 57:34–41. https://doi.org/10.1016/j.tice.2019.02.003
Datta S, Ghosh D, Saha DR et al (2009) Chronic exposure to low concentration of arsenic is immunotoxic to fish: role of head kidney macrophages as biomarkers of arsenic toxicity to Clarias batrachus. Aquat Toxicol 92:86–94. https://doi.org/10.1016/j.aquatox.2009.01.002
de Oliveira SE, de Costa P, M, Nascimento SB do, et al (2018) Atrazine promotes immunomodulation by melanomacrophage centre alterations in spleen and vascular disorders in gills from Oreochromis niloticus. Aquat Toxicol. https://doi.org/10.1016/j.aquatox.2018.06.018
Dzik AJ (2018) Nuuk, Greenland: site, situation, and “the law of the primate city”. North Rev 48:3–32. https://doi.org/10.22584/nr48.2018.001
Evans D, Nowak B (2016) Effect of ranching time on melanomacrophage centres in anterior kidney and spleen of southern bluefin tuna, Thunnus maccoyii. Fish Shellfish Immunol 59:358–364
Fedorov VV (1986) Cottidae. In: Whitehead PJP, Bauchot M-L, Hureau J-C, Nielsen J, Tortonese E (eds) Fishes of the North-eastern Atlantic and the Mediterranean, Unesco. Unesco, Paris, pp 1243–1260
Ferreira CMH (2011) Can fish liver melanomacrophages be modulated by xenoestrogenic and xenoandrogenic pollutants? Experimental studies on the influences of temperature, sex, and ethynylestradiol, using the platyfish as the model organism. Dissertation, Universidade do Porto
Fournie JW, Summers JK, Courtney LA et al (2001) Utility of splenic macrophage aggregates as an indicator of fish exposure to degraded environments. J Aquat Anim Health 13:105–116
Galindo-Villegas J, Garcia-Alcazar A, Meseguer J, Mulero V (2019) Aluminum adjuvant potentiates gilthead seabream immune responses but induces toxicity in splenic melanomacrophage centers. Fish Shellfish Immunol 85:31–43. https://doi.org/10.1016/j.fsi.2018.02.047
Ghosh D, Datta S, Bhattacharya S, Mazumder S (2007) Long-term exposure to arsenic affects head kidney and impairs humoral immune responses of Clarias batrachus. Aquat Toxicol 81:79–89
Giari L, Manera M, Simoni E, Dezfuli BS (2007) Cellular alterations in different organs of European sea bass Dicentrarchus labrax ( L.) exposed to cadmium. Chemosphere 67:1171–1181
Girard (1849) Acanthocottus. In Jordan DS, Evermann BW, Clark HW (1930) Check list of the fish and fishlike vertebrates of North and Middle America north of the northern boundary of Venezuela and Columbia. Rept US Comm Fish 1928 part 2 386
Government of Greenland (2014) Greenlands oil and mineral strategy 2014–2018 Government of Greenland February 2014. 102. https://www.govmin.gl/images/stories/about_bmp/publications/Greenland_oil_and_mineral_strategy_2014–2018_ENG.pdf
Graves SD, Kidd KA, Houlahan JE, Munkittrick KR (2017) General and histological indicators of health in wild fishes from a biological mercury hotspot in northeastern North America. Environ Toxicol Chem 36:976–987
Hansson S, Bengtsson B-E, Bengtsson Å (1984) Stomach contents in Baltic fourhorn sculpin (Myoxocephalus quadricornis L.) with normal and deformed spinal vertebrae. Mar Pollut Bull 15:375–377
Harrad SJ, Sewart AP, Alcock R et al (1994) Polychlorinated biphenyls (PCBs) in the British environment: Sinks, sources and temporal trends. Environ Pollut 85:131–146
Hinck JE, Blazer VS, Denslow ND et al (2007) Biomarkers of contaminant exposure in northern pike (Esox lucius) from the Yukon River Basin, Alaska. Arch Environ Contam Toxicol 52:549–562
Hylland K (2006) Polycyclic aromatic hydrocarbon (PAH) ecotoxicology in marine ecosystems. J Toxicol Environ Health 69:109–123. https://doi.org/10.1080/15287390500259327
Jacobsen J, Asmund G (2000) TBT in marine sediments and blue mussels (Mytilus edulis) from central-west Greenland. Sci Total Environ 245:131–136. https://doi.org/10.1016/S0048-9697(99)00438-6
Jordanova M, Rebok K, Naskovska M et al (2016) Splenic pigmented macrophage aggregates in barbel (Barbus peloponnesius, Valenciennes, 1844) from river Bregalnica — Influences of age, sex and season on a pollution biomarker. Turkish J Fish Aquat Sci 16:881–890. https://doi.org/10.4194/1303-2712-v16
Kaarsholm HM, Verland N, Nørregaard RD et al (2019) Histology of sculpin spp. in East Greenland. II. Histopathology and trace element concentrations. Toxicol Environ Chem 2248:1–16. https://doi.org/10.1080/02772248.2019.1579992
Kranz H (1986) Symposium Toxic Chemicals and Aquatic Life: Research and Management. Seattle, Washington
Kranz H, Gercken J (1987) Effects of sublethal concentrations of potassium dichromate on the occurrence of splenic melano-macrophage centres in juvenile plaice, Pleuronectes platessa, L. J Fish Biol 31:75–80
Lam PKS (2009) Use of biomarkers in environmental monitoring. Ocean Coast Manag 52:348–354. https://doi.org/10.1016/j.ocecoaman.2009.04.010
Lam PKS, Gray JS (2003) The use of biomarkers in environmental monitoring programmes. Mar Pollut Bull 46:182–186
Leonardsson K, Bengtsson Å, Linnér J (1988) Size-selective predation by fourhorn sculpin, Myoxocephalus quadricornis (L.) (Pisces) on Mesidotea entomon (L.) (Crustacea, Isopoda). Hydrobiologia 164:213–220
Manera M, Serra R, Isani G, Carpené E (2000) Macrophage aggregates in gilthead sea bream fed copper, iron and zinc enriched diets. J Fish Biol 57:457–465
Matsche MA, Blazer VS, Virginia W, Mazik PM (2019) Comparisons of stereological and other approaches for quantifying macrophage aggregates in piscine spleens. J Aquat Anim Health 31:1–21. https://doi.org/10.1002/aah.10086
Matthiessen P, Roberts RJ (1982) Histopathological changes in the liver and brain of fish exposed to endosulfan insecticide during tsetse fly control operations in Botswana. J Fish Dis 5:153–159. https://doi.org/10.1111/j.1365-2761.1982.tb00468.x
Mela M, Randi MAF, Ventura DF et al (2007) Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias malabaricus. Ecotoxicol Environ Saf 68:426–435
Miranda AL, Roche H, Randi MAF et al (2008) Bioaccumulation of chlorinated pesticides and PCBs in the tropical freshwater fish Hoplias malabaricus: Histopathological, physiological, and immunological findings. Environ Int 34:939–949
Morrow JE (1980) The freshwater fishes of Alaska. Alaska Northwest Pub. Co
Nørregaard RD, Dang M, Bach L et al (2018) Comparison of heavy metals, parasites and histopathology in sculpins (Myoxocephalus spp.) from two sites at a lead-zinc mine in North East Greenland. Environ Res 165:306–316. https://doi.org/10.1016/j.envres.2018.04.016
Patey G, Couillard CM, Pierron F, Baudrimont M (2017) Biotransformation, antioxidant and histopathological biomarker responses to contaminants in European and American yellow eels from the Gironde and St. Lawrence Estuaries. Chemosphere 188:292–303. https://doi.org/10.1016/j.chemosphere.2017.08.139
Payne JF, Fancey LF (1989) Effect of polycyclic aromatic hydrocarbons on immune responses in fish: change in melanomacrophage centers in flounder (Pseudopleuronectes americanus) exposed to hydrocarbon-contaminated sediments. Mar Environ Res 28:431–435
Qualhato G, Maria S, De S-M, Damacena L (2018) Melanomacrophage response and hepatic histopathologic biomarkers in the guppy Poecilia reticulata exposed to iron oxide (maghemite) nanoparticles. Aquat Toxicol 198:63–72. https://doi.org/10.1016/j.aquatox.2018.02.014
Rabitto IS, Alves Costa JRM, Silva De Assis HC et al (2005) Effects of dietary Pb(II) and tributyltin on neotropical fish, Hoplias malabaricus: Histopathological and biochemical findings. Ecotoxicol Environ Saf 60:147–156
Rhea DT, Farag AM, Harper DD et al (2013) Mercury and selenium concentrations in biofilm, macroinvertebrates, and fish collected in the yankee fork of the Salmon River, Idaho, USA, and their potential effects on fish health. Arch Environ Contam Toxicol 64:130–139. https://doi.org/10.1007/s00244-012-9816-x
Ribeiro HJ, Procópio MS, Gomes JMM et al (2011) Functional dissimilarity of melanomacrophage centres in the liver and spleen from females of the teleost fish Prochilodus argenteus. Cell Tissue Res 346:417–425. https://doi.org/10.1007/s00441-011-1286-3
Riger-Kusk O, Gregor O (2013) Udvidelse Af Havnen I Nuuk Vvm-Redegørelse (expansion of the port in Nuuk EIA statement). Nuuk
Robins CR, Ray C (1986) A field guide to Atlantic Coast fishes: North America. Houghton Mifflin Harcourt
Sayed AEDH (2016) Genotoxicity detection following exposure to silver nanoparticles in African catfish (Clarias gariepinus). Int J Nanoparticles 9:41–53
Sayed AH, Younes HAM (2017) Melanomacrophage centers in Clarias gariepinus as an immunological biomarker for toxicity of silver nanoparticles. J Microsc Ultrastruct 5:97–104. https://doi.org/10.1016/j.jmau.2016.07.003
Sayed AE-DH, Abd-Elkareem M, Abou Khalil NS (2019) Immunotoxic effects of 4-nonylphenol on Clarias gariepinus: cytopathological changes in hepatic melanomacrophages. Aquat Toxicol 207:83–90. https://doi.org/10.1016/j.aquatox.2018.12.002
Scott WB, Scott MG (1988) Atlantic fishes of Canada. Published by the University of Toronto Press in cooperation with the Minister of Fisheries and Oceans and the Canadian Government Publishing Centre, Supply and Services Canada
Søndergaard J, Halden N, Bach L et al (2015) Otolith chemistry of common sculpins (Myoxocephalus scorpius) in a mining polluted Greenlandic fiord (Black Angel lead-zinc mine, West Greenland). Water Air Soil Pollut 226:1–12. https://doi.org/10.1007/s11270-015-2605-1
Sonne C, Bach L, Søndergaard J et al (2014) Evaluation of the use of common sculpin (Myoxocephalus scorpius) organ histology as bioindicator for element exposure in the fjord of the mining area Maarmorilik, West Greenland. Environ Res 133:304–311
Stosik MP, Tokarz-deptuła B, Deptuła W (2019) Melanomacrophages and melanomacrophage centres in Osteichthyes. Cent Eur J Immunol 44:201–205
Strand J, Asmund G (2003) Tributyltin accumulation and effects in marine molluscs from West Greenland. Environ Pollut 123:31–37. https://doi.org/10.1016/S0269-7491(02)00361-5
Vigliano FA, Bermúdez R, Quiroga MI, Nieto JM (2006) Evidence for melano-macrophage centres of teleost as evolutionary precursors of germinal centres of higher vertebrates: An immunohistochemical study. Fish Shellfish Immunol 21:467–471. https://doi.org/10.1016/j.fsi.2005.12.012
Vorkamp K, Strand J, Christensen JH et al (2010) Polychlorinated biphenyls, organochlorine pesticides and polycyclic aromatic hydrocarbons in a one-off global survey of bivalves. J Environ Monit 12:1141–1152. https://doi.org/10.1039/b918998j
Weeks BA, Warinner JE, Mason PL, McGinnis DS (1986) Influence of toxic chemicals on the chemotactic response of fish macrophages. J Fish Biol 28:653–658
Westin L (1970) The food ecology and the annual food cycle in the Baltic population of four-horn sculpin (Myoxocephalus quadricornis L.) Pisces. Inst Freshw Res Drottningholm, Rep 50:168–210
Funding
The University of Tasmania is acknowledged for funding Mai Dang’s PhD scholarship and supporting her research. The Ministry of Environment and Food, Denmark and the Environmental Agency for Mineral Resources Activities, Greenland is acknowledged for supporting the field trip by which our archival samples were collected.
Author information
Authors and Affiliations
Contributions
MD: conceptualization; data analysis; methodology; validation; visualization; investigation, writing—original draft; writing—review and editing. RN: sample collection, investigation, writing—review and editing. CS: investigation, resources, funding acquisition, writing—review and editing. LB: investigation, resources, funding acquisition, writing—review and editing. MS: investigation, resources, writing—review and editing, supervision. KJ: investigation, writing—review and editing. BN: conceptualization, investigation, resources, writing—review and editing, supervision, project administration, funding acquisition.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
We used archival samples in this study, collected previously for other studies. Therefore, ethic approval is waiver for this study. The collection method (described in this paper) was according to Greenland regulations and conducted by a FELASA certificated member (FELASA Accreditation No 32/10/288).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Dang, M., Nørregaard, R., Sonne, C. et al. Splenic and renal melanomacrophage centers in shorthorn sculpins (Myoxocephalus scorpius) in Nuuk harbor, West Greenland. Polar Biol 44, 2011–2021 (2021). https://doi.org/10.1007/s00300-021-02934-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-021-02934-0