Abstract
The marine environment is increasingly polluted by anthropogenic wastes, notably plastic debris. This debris breaks down into smaller pieces, known as microplastics. When consumed by marine organisms, microplastics cause various physiological effects. In this study, we sought to determine a link between ingested microplastics and cytochrome P450-1A (CYP1A) expression in fish liver. To achieve this goal, we collected pinfish from five sites in Lower Laguna Madre (LLM, a large coastal lagoon), analyzed stomach contents, excised liver tissues, and performed immunohistochemical analysis to determine CYP1A expression. Microplastics were not discovered in the stomach/intestine of pinfish, though plastic debris was present at various stages of decomposition within sampling sites. Hepatic CYP1A expression was significantly higher in pinfish collected from four of five sampling sites when compared to fish in laboratory conditions. These results imply that pinfish, as well as other organisms, may be exposed to pollutants other than microplastics in LLM.
Similar content being viewed by others
Data availability
The data of this study are available from the corresponding author upon request.
Abbreviations
- CYP1A:
-
Cytochrome P450-1A
- PCBs:
-
Polychlorinated biphenyls
- PCDDs:
-
Polychlorinated dibenzodioxins
- PCDFs:
-
Polychlorinated dibenzofurans
- BPA:
-
Bisphenol A
- PAHs:
-
Polycyclic aromatic hydrocarbons
References
Agamy E (2012) Histopathological liver alterations in juvenile rabbit fish (Siganus canaliculatus) exposed to light Arabian crude oil, dispersed oil and dispersant. Ecotoxicol Environ Saf 75(1):171–179. https://doi.org/10.1016/j.ecoenv.2011.09.010
Al-Ghai SM (2013) Acetylcholinesterase, glutathione and hepatosomatic index as potential biomarkers of sewage pollution and depuration in fish. Mar Pollut Bull 74(1):183–186. https://doi.org/10.1016/j.marpolbul.2013.07.005
Alomar C, Sureda A, Capo X, Tejada S, Deudero S (2017) Microplastics ingestion by Mullus surmuletus Linnaeus, 1758 fish and its potential for causing oxidative stress. Environ Res 159:135–142. https://doi.org/10.1016/j.envres.2017.07.043
Andrady AL (2011) Microplastics in the marine environment. Mar Pollut Bull 62(8):1596–1605. https://doi.org/10.1016/j.marpolbul.2011.05.030
Batel A, Linti F, Scherer M, Erdinger L, Braunbeck T (2016) Transfer of benzo[a]pyrene from microplastics to Artemia nauplii and further to zebrafish via a trophic food web experiment: CYP1A induction and visual tracking of persistent organic pollutants. Environ Toxicol Chem 35(7):1656–1666. https://doi.org/10.1002/etc.3361
Bishop MJ, Wear SL (2005) Ecological consequences of ontogenetic shifts in predator diet: seasonal constraint of a behaviorally mediated indirect interaction. J Exp Mar Biol Ecol 326(2):199–206. https://doi.org/10.1016/j.jembe.2005.05.017
Bolger T, Connolly PL (1989) The selection of suitable indices for the measurement and analysis of fish condition. J Fish Biol 34(2):171–182. https://doi.org/10.1111/j.1095-8649.1989.tb03300.x
Brammell BF, McClain JS, Oris JT, Price DJ, Birge WJ, Elskus AA (2010) CYP1A expression in caged rainbow trout discriminates among sites with various degrees of polychlorinated biphenyl contamination. Arch Environ Contam Toxicol 58(3):772–782. https://doi.org/10.1007/s00244-009-9368-x
Buckland A, Baker R, Loneragan N, Sheaves M (2017) Standardising fish stomach content analysis: the importance of prey condition. Fish Res 196:126–140. https://doi.org/10.1016/j.fishres.2017.08.003
Bugica K, Sterba-Boatwright B, Wetz MS (2020) Water quality trends in Texas estuaries. Mar Pollut Bull 152:110903. https://doi.org/10.1016/j.marpolbul.2020.110903
Cedervall T, Hansson LA, Lard M, Frohm B, Linse S (2012) Food chain transport of nanoparticles affects behaviour and fat metabolism in fish. PLoS One 7(20):e32254. https://doi.org/10.1371/journal.pone.0032254
Chavan VR, Muley DV (2014) Effect of heavy metals on liver and gill of fish Cirrhinus mrigala. Int J Curr Microbiol App Sci 3(5):277–288. https://doi.org/10.1590/1678-4324-2016150275
Chiang J (2014) Liver physiology: metabolism and detoxification. In: McManus LM, Mitchell RN (eds) Pathobiology of human diseases. Elsevier, San Diego, pp 1770–1782
Chipps SR, Garvey JE (2007) Assessment of diets and feeding patterns. In: Guy C, Brown (eds) Analysis and interpretation of freshwater fisheries data, Chapter 11. American Fisheries Society, Bethesda, Maryland, pp 1–41 file:///C:/Users/usg319/Downloads/Chapter11ChippsandGarvey%20(1).pdf
Choi JS, Jung YJ, Hong SH, Park JW (2018) Toxicological effects of irregularly shaped and spherical microplastics in a marine teleost, the sheepshead minnow (Cyprinodon variegatus). Mar Pollut Bull 129(1):231–240. https://doi.org/10.1016/j.marpolbul.2018.02.039
Custer TW, Mitchell CA (1993) Trace elements and organochlorines in the shoalgrass community of the Lower Laguna Madre, Texas. Environ Monit Assess 25:235–246. https://doi.org/10.1007/BF00548024
de Sá LC, Luis LG, Guilhermino L (2015) Effects of microplastics on juveniles of the common goby (Pomatoschistus microps): confusion with prey, reduction of the predatory performance and efficiency, and possible influence of development conditions. Environ Pollut 196:359–362. https://doi.org/10.1016/j.envpol.2014.10.026
de Sales-Ribero C, Brito-Casillas Y, Fernandez A, Caballero MJ (2020) An end to the controversy over the microscopic detection and effects of pristine microplastics in fish organs. Sci Rep 10:12434. https://doi.org/10.1038/s41598-020-69062-3
Dubansky B, Rice CD, Barrois LF, Galvez F (2017) Biomarkers of aryl-hydrocarbon receptor activity in Gulf Killifish (Fundulus grandis) from northern Gulf of Mexico marshes following the Deepwater Horizon oil spill. Arch Environ Contam Toxicol 73:63–75. https://doi.org/10.1017/s00244-017-0417-6
Frank WJ, Richard C, Bartlett RD, John WC (2002) The Laguna Madre of Texas and Tamaulipas (Gulf Coast studies series, 2). Texas A&M University Press, College Station
Griet V, Lisbeth VC, Colil RJ, Antonio M, Kit G, Gabriella F, Michel KJJ, Jorge D, Karen B, Johan R, Lisa D (2015) A critical view on microplastic quantification in aquatic organisms. Environ Res 143:46–55. https://doi.org/10.1016/j.envres.2015.07.016
Hankinson O (1995) The aryl hydrocarbon receptor complex. Annu Rev Pharmacol Toxicol 35:307–340
Harris R, Pollman C, Landing W, Evans D, Axelrad D, Hutchinson D, Morey SL, Rumbold D, Dukhovskoy D, Adams DH, Vijayaraghavan K, Holmes C, Atkinson RD, Myers T, Sunderland E (2012) Mercury in the Gulf of Mexico: sources to receptors. Environ Res 119:42–52. https://doi.org/10.1016/j.envres.2012.08.001
Hellou J, Lebeuf M, Rudi M (2013) Review on DDT and metabolites in birds and mammals of aquatic ecosystems. Environ Rev 21:53–69. https://doi.org/10.1139/er-2012-0054
Jordan F, Bartolini M, Nelson C, Patterson PE, Soulen HL (1997) Risk of predation affects habitat selection by the pinfish Lagodon rhomboides (Linnaeus). J Exp Mar Biol Ecol 208(1–2):45–56. https://doi.org/10.1016/S0022-0981(96)02656-1
Klak GE (1941) The condition of brook trout and rainbow trout from four Eastern streams. Trans Am Fish Soc 70(1):282–289. https://doi.org/10.1577/1548-8659(1940)70[282:TCOBTA]2.0.CO;2
Linhoss AC, Camacho R, Ashby S (2016) Oyster habitat suitability in the northern Gulf of Mexico. J Shellfish Res 35(4):841–849
Luczkovich JJ, Stellwag EJ (1993) Isolation of cellulolytic microbes from the intestinal tract of the pinfish, Lagodon rhomboides: size-related changes in diet and microbial abundance. Mar Biol 116:381–388
Lusher L, McHugh M, Thompson RC (2013) Occurrence of microplastics in the gastrointestinal tract of pelagic and demersal fish from the English Channel. Mar Pollut Bull 67(1–2):94–99. https://doi.org/10.1016/j.marpolbul.2012.11.028
Mahesh V, Gop A, Nair RJ (2018) Stomach content analysis techniques in fishes. In: Nair RJ, Gop AP, Mahesh (eds) Recent advances in fishery biology techniques for biodiversity evaluation and conservation. Central Marine Fisheries Research Institute, Kochi (India), pp 104–115 https://www.researchgate.net/publication/330621031
Mela M, Randi MAF, Ventura DE, Carvalho CEV, Pelletier E, Oliveira Ribeiro CA (2007) Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias malabaricus. Ecolotoxicol. Environ Saf 68:426–435. https://doi.org/10.1016/j.ecoenv.2006.11.013
Mishra VK, Upadhyay AR, Pandey SK, Tripathi BD (2008) Concentrations of heavy metals and aquatic macrophytes of Govind Ballabh Pant Sagar an anthropogenic lake affected by coal mining effluent. Environ Monit Assess 141:49–58. https://doi.org/10.1007/s10661-007-9877-x
Moore CJ (2008) Synthetic polymers in the marine environment: a rapidly increasing, long-term threat. Environ Res 108(2):131–139. https://doi.org/10.1016/j.envres.2008.07.025
Moreno T, Querol X, Alastuey A, Cruz Minguillo M, Pey J, Rodriguez S, Miro JV, Felis C, Gibbons W (2007) Recreational atmospheric pollution episodes: inhalable metalliferous particles from firework displays. Atmos Environ 41:913–922. https://doi.org/10.1016/j.atmosenv.2006.09.019
Ortiz-Delgado J, Sarasquete C, Behrens A, González de Canales M, Segner H (2002) Expression, cellular distribution and induction of cytochrome P4501A (CYP1A) in gilthead seabream, Sparus aurata, brain. Aquat Toxicol 60(3):269–283. https://doi.org/10.1016/S0166-445X(02)00006-1
Oziolor EM, Apell JN, Windfield ZC, Back JA, Usenko S, Matson CW (2018) Polychlorinated biphenyl (PCB) contamination in Galveston Bay, Texas: comparing concentrations and profiles in sediments, passive samplers, and fish. Environ Pollut 236:609–618. https://doi.org/10.1016/j.envpol.2018.01.086
Phillips MB, Bonner TH (2015) Occurrence and amount of microplastic ingested by fishes in watersheds of the Gulf of Mexico. Mar Pollut Bull 100(1):264–269. https://doi.org/10.1016/j.marpolbul.2015.08.041
Pickering H, Whitmarsh D (1997) Artificial reefs and fisheries exploitation: a review of the “attraction versus production” debate, the influence of design and its significance for policy. Fish Res 31(1–2):39–59. https://doi.org/10.1016/S0165-7836(97)00019-2
Rahman MS, Thomas P (2012) Effects of hypoxia exposure on hepatic cytochrome P450 1A (CYP1A) expression in Atlantic croaker: molecular mechanisms of CYP1A down-regulation. PLoS One 7(7):e40825. https://doi.org/10.1371/journal.pone.0040825
Rahman MS, Thomas P (2018) Interactive effects of hypoxia and PCB co-exposure on expression of CYP1A and its potential regulators in Atlantic croaker liver. Environ Toxicol 33:411–421. https://doi.org/10.1002/tox.22527
Rice CD, Schlenk D, Ainsworth J, Goksøyr A (1998) Cross-reactivity of monoclonal antibodies against peptide 277–294 of rainbow trout CYP1A1 with hepatic CYP1A among fish. Mar Envrion Res 46(1–5):87–91. https://doi.org/10.1016/S0141-1136(97)00122-0
Rochman CM, Hoh E, Kurobe T, Teh SJ (2013) Ingested plastic transfers hazardous chemicals to fish and induces hepatic stress. Sci Rep 3:3263. https://doi.org/10.1038/srep03263
Rochman CM, Tahir A, Williams SL, Baxa DV, Lam R, Miller JT, Teh FC, Werorilangi TSJ (2015) Anthropogenic debris in seafood: plastic debris and fibers from textiles in fish and bivalves sold for human consumption. Sci Rep 5:14340. https://doi.org/10.1038/srep14340
Sarasquete C, Segner H (2000) Cytochrome P4501A (CYP1A) in teleostean fishes. A review of immunohistochemical studies. Sci Total Environ 247:313–332. https://doi.org/10.1016/s0048-9697(99)00500-8
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Stunz G, Robillard M (2011) Contaminant level of fishes in several coastal bend estuaries: screening investigation. In: Technical Report, Heart Research Institute for Gulf of Mexico Studies, Coastal Bend Bays & Estuaries Program. Texas A&M University - Corpus Christi, Texas Retrieved from: https://www.cbbep.org/publications/virtuallibrary/1012.pdf
Tolan JM, Holt SA, Onuf CP (1997) Distribution and community structure of ichthyoplankton in Laguna Madre seagrass meadows: potential impact of seagrass species change. Estuaries 20:450–464
Vázquez OA, Rahman MS (2021) An ecotoxicological approach to microplastics on terrestrial and aquatic organisms: a systematic review in assessment, monitoring and biological impact. Environ Toxicol Pharmacol 84:103615. https://doi.org/10.1016/j.etap.2021.103615
Whelan T, Espinoza J, Villarreal X, CottaGoma M (2005) Trace metal partitioning in Thalassia testudinum and sediments in the Lower Laguna Madre, Texas. Environ Int 31:15–24. https://doi.org/10.1016/j.envint.2004.05.010
Zacharia PU, Abdurahiman KP (2003) Methods of stomach content analysis of fishes. Winter School on Towards Ecosystem Based Managwement of Marine Fisheries - Building- Mass Balance Tropic and Simulation Models. In: Technical notes. Centeral Marine Fisheries Research Institute (CMFRI), Cochin, Kerala, India http://eprints.cmfri.org.in/5282/1/19.pdf
Zapata-Perez O, Sanchez-Teyer LF, Perez-Nunez MT, Arroyo-Herrera AL, Moreno AQ, Albores-Medina AA (2010) Response of CYP1A gene expression in fish live of catfish (Ariopsis felis) from Gulf of Mexico and their relationship with the genetic variability. J Environ Sci Health A 45A:62–67. https://doi.org/10.1080/10934520903388830
Acknowledgements
We would like to thank the Texas Park & Wildlife Department for allowing us to collect pinfish, and David Tran, UTRGV, for the valuable comments and suggestions on the manuscript. We would also like to thank and greatly appreciate three anonymous reviewers for providing their valuable suggestions and constructive comments on the manuscript.
Funding
This study was supported by grants from the NOAA marine debris education program to Abdullah Faiz Rahman (Clean Valley-Clean Gulf: A Marine Debris Prevention Program for the Rio Grande Valley, grant no. NA15NOS4630153) and in part by the start-up fund and UTRGV College of Science SEED grant (grant no. 210000371) to Md Saydur Rahman.
Author information
Authors and Affiliations
Contributions
Md Saydur Rahman gave the research idea. Md Saydur Rahman and Abdullah Faiz Rahman supervised research. Stephanie DuBois conducted field and laboratory studies and collected and analyzed data. Stephanie DuBois and Md Saydur Rahman designed the figures. Stephanie DuBois and Brittney Lacy drafted the manuscript. Stephanie DuBois, Brittney Lacy, Abdullah Faiz Rahman, and Md Saydur Rahman edited and reviewed the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Fish were collected in the LLM lagoon according to the approved wild-caught species regulations of the Texas Parks & Wildlife Department (permit number: SPR-0913-125). Fish were transported with aerated seawater to UTRGV Coastal campus lab and treated in accordance with the standard handling and experiment protocol approved by the UTRGV Institutional Animal Care and Use Committee (protocol number: 2016-010-IACUC).
Consent for publication
All the authors have read and approved to submit the final version of the manuscript.
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Cinta Porte
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
DuBois, S., Lacy, B., Rahman, A.F. et al. Elevated CYP1A expression detected in pinfish collected from a coastal lagoon in the southern Texas Gulf Coast: indicative of exposure to microplastics or pollutants?. Environ Sci Pollut Res 28, 32066–32073 (2021). https://doi.org/10.1007/s11356-021-14351-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-14351-1