Abstract
Fish development can be affected by environmental pollutants such as crude oil (anthropogenic or natural sources), causing alterations especially in cardiac function and morphology. Most such studies have focused on saltwater species, whereas studies in freshwater fishes are scant. The objective of the current study was to evaluate the effects of crude oil exposure (as 0, 5, 10, 15, or 20% high-energy water accommodated fractions, HEWAF) on cardiac function and edema formation during two early periods of development (embryo and eleuteroembryo, 48 h each) individually using the tropical gar Atractosteus tropicus as a model. Embryos did not exhibit alterations in body mass, total length, condition factor, and cardiac function as a function of oil. In contrast, eleuteroembryos proved to be more sensitive and exhibited increased body mass, total length, and condition factor, decreased heart rate and phenotypic alterations such as cardiac dysmorphia (tubular hearts) and spine curvature at high concentrations of HEWAF. Moreover, edema formation was observed in both stages This study shows different functional responses of A. tropicus after crude oil exposure and provides useful information of the developmental impacts of these compounds on the early life stages of freshwater tropical fishes.
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References
Abbas O, Rebufa C, Dupuy N, Permanyer A, Kister J (2008) Assessing petroleum oils biodegradation by chemometric analysis of spectroscopic data. Talanta 75(4):857–871. https://doi.org/10.1016/j.talanta.2007.12.027
Abdel-Shafy HI, Mansour MS (2016) A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J Pet 25(1):107–123. https://doi.org/10.1016/j.ejpe.2015.03.011
Aguilera C, Mendoza R, Rodríguez G, Márquez G (2002) Morphological description of alligator gar and tropical gar larvae, with an emphasis on growth indicators. Trans Am Fish Soc 131(5):899–909. https://doi.org/10.1577/15488659(2002)131<0899:MDOAGA>2.0.CO;2
Anderson BS, Arenella-Parkerson D, Phillips BM, Tjeerdema RS, Crane D (2009) Preliminary investigation of the effects of dispersed Prudhoe Bay Crude Oil on developing top smelt embryos, Atherinops affinis. Environ Pollut 157(3):1058–1061. https://doi.org/10.1016/j.envpol.2008.10.013
Asemani M, Rabbani AR (2016) Oil-oil correlation by FTIR spectroscopy of asphaltene simples. Geosci J 20:273–283. https://doi.org/10.1007/s12303-015-0042-1
Baali A, Yahyaoui A (2020) Polycyclic aromatic hydrocarbons (PAHs) and their influence to some aquatic species. In Biochemical Toxicology – Heavy Metals and Nanomaterials. IntechOpen. https://doi.org/10.5772/intechopen.86213
Barron MG, Carls MG, Short JW, Rice SD (2003) Photoenhanced toxicity of aqueous phase and chemically dispersed weathered Alaska North Slope crude oil to Pacific herring eggs and larvae. Environ Toxicol Chem 22(3):650–660. https://doi.org/10.1002/etc.5620220326
Bautista NM, Burggren WW (2019) Parental stressor exposure simultaneously conveys both adaptive and maladaptive larval phenotypes through epigenetic inheritance in the zebrafish (Danio rerio). J Exp Biol 222(17):jeb208918. https://doi.org/10.1242/jeb.208918
Bender ML, Fratzen M, Camus L, Le Floch S, Palerud J, Nahrgang J (2018) Effects of acute exposure to dispersed oil and burned oil residue on long-term survival, growth, and reproductive development in polar cod (Boreogadus saida). Mar Environ Res 148:468–477. https://doi.org/10.1016/j.marenvres.2018.09.005
Bosker T, van Balen L, Walsh B, Sepúlveda MS, DeGuise S, Perkins C, Griffitt RJ (2017) The combined effect of Macondo oil and corexit on sheepshead minnow (Cyprinodon variegatus) during early development. J Toxicol Environ Health Part A 80(9):477–484. https://doi.org/10.1080/15287394.2017.1340208
Brette F, Shiels HA, Galli GLJ, Cros C, Incardona JP, Scholz NL, Block BA (2017) A novel cardiotoxic mechanism for a pervasive global pollutant. Sci Rep 7:41476. https://doi.org/10.1038/srep41476
Brown-Peterson NJ, Krasnec M, Takeshita R, Ryan CN, Griffitt KJ, Lay C, Mayer GD, Bayha KM, Hawkins WE, Lipton I, Morris J, Griffitt RJ (2015) A multiple endpoint analysis of the effects of chronic exposure to sediment contaminated with Deepwater Horizon oil on juvenile Southern flounder and their associated microbiomes. Aquat Toxicol 165:197–209. https://doi.org/10.1016/j.aquatox.2015.06.001
Brown-Peterson NJ, Krasnec MO, Lay CR, Morris JM, Griffitt RJ (2017) Responses of juvenile southern flounder exposed to Deepwater Horizon oil-contaminated sediments. Environ Toxicol Chem 36(4):1067–1076. https://doi.org/10.1002/etc.3629
Burggren WW (2005) Developing animals flout prominent assumptions of ecological physiology. Comp Biochem Physiol 141C:430–439. https://doi.org/10.1016/j.cbpb.2005.03.010
Burggren WW, Bagatto B (2008) Cardiovascular anatomy and physiology. In: Finn RN, Kapoor BJ (eds) In Fish Larval Physiology. Science Publishers, Enfield, pp 119–161
Burggren WW, Dubansky B (2018) Development and Environment. Springer, Cham
Burggren WW, Martínez-Bautista G, Camarillo-Coop SC, Márquez-Couturier G, Páramo-Delgadillo S, Martínez-García R, Alvarez-González CA (2016) Developmental cardiorespiratory physiology of the air-breathing tropical gar, Atractosteus tropicus. Am J Physiol-Reg I 311(4):R689–R701. https://doi.org/10.1152/ajpregu.00022.2016
Carls MG, Rice SD, Hose JE (1999) Sensitivity of fish embryos to weathered crude oil: Part I. Low-level exposure during incubation causes malformations, genetic damage, and mortality in larval Pacific herring (Clupea pallasi). Environ Toxicol Chem 18(3):481–493. https://doi.org/10.1002/etc.5620180317
Carls MG, Holland L, Larsen M, Collier TK, Scholz NL, Incardona JP (2008) Fish embryos are damaged by dissolved PAHs, not oil particles. Aquat Toxicol 88(2):121–127. https://doi.org/10.1016/j.aquatox.2008.03.014
Carney SA, Prash AL, Heideman W, Peterson RE (2006) Understanding dioxin developmental toxicity using the zebrafish model. Birth Defects Res Part A Clin Mol Teratol 76:7–18. https://doi.org/10.1002/BDRA.20216
Cherr GN, Fairbairn E, Whitehead A (2017) Impacts of petroleum-derived pollutants on fish development. Annu Rev Anim Biosci 5:185–203. https://doi.org/10.1146/annurev-animal-022516-022928
Comabella Y, Hurtado A, Canabal J, García-Galano T (2014) Effect of temperature on hatching and growth of Cuban gar (Atractosteus tristoechus) larvae. Ecosistemas y Recursos Agropecuarios 1(1):19–32
de Soysa TY, Ulrich A, Friedrich T, Pite D, Compton SL, Ok D, Lagdameo MC (2012) Macondo crude oil from the Deepwater Horizon oil spill disrupts specific developmental processes during zebrafish embryogenesis. BMC Biol 10(1):1–25. https://doi.org/10.1186/1741-7007-10-40
Del Río AM, Davis BE, Fangue NA, Todgham AE (2019) Combined effects of warming and hypoxia on early life stage Chinook salmon physiology and development. Conserv Physiol 7(1):coy078. https://doi.org/10.1093/conphys/coy078
Duffy TA, Childress W, Portier R, Chesney EJ (2016) Responses of bay anchovy (Anchoa mitchilli) larvae under lethal and sublethal scenarios of crude oil exposure. Ecotoxicol Environ Saf 134P1:264–272. https://doi.org/10.1016/j.ecoenv.2016.08.010
Dzul-Caamal R, Salazar-Coria L, Olivares-Rubio HF, Rocha-Gómez MA, Girón-Pérez MI, Vega-López A (2016) Oxidative stress response in the skin mucus layer of Goodea gracilis (Hubbs and Turner, 1939) exposed to crude oil: a non-invasive approach. Comp Biochem Physiol A 200:9–20. https://doi.org/10.1016/j.cbpa.2016.05.008
Eddy FB, Handy RD (2012) Ecological and environmental physiology of fishes, 1st edn. Oxford University Press, Oxford, p 264. https://doi.org/10.1111/jfb.12106
Edmunds RC, Gill JA, Baldwin DH, Linbo TL, French BL, Brown TL, Benetti D (2015) Corresponding morphological and molecular indicators of crude oil toxicity to the developing hearts of mahi mahi. Sci Rep 5:17326. https://doi.org/10.1038/srep17326
Esbaugh AJ, Mager EM, Stieglitz JD, Hoenig R, Brown TL, French BL, Linbo TL, Lay C, Forth H, Scholz NL, Incardona JP, Morris JM, Benetti DD, Grosell M (2016) The effects of weathering and chemical dispersion on Deepwater Horizon crude oil toxicity to mahi-mahi (Coryphaena hippurus) early life stages. Sci Total Environ 543:644–651. https://doi.org/10.1016/j.scitotenv.2015.11.068
Faria M, Bedrossiantz J, Prats E, Garcia XR, Gómez-Canela C, Piña B, Raldúa D (2019) Deciphering the mode of action of pollutants impairing the fish larvae escape response with the vibrational startle response assay. Sci Total Environ 672:121–128. https://doi.org/10.1016/j.scitotenv.2019.03.469
Finn RN, Kapoor BG (2008) Fish larval physiology. Science Publishers, Enfield. https://doi.org/10.1086/650279
Froese R (2006) Cube law, condition factor and weight–length relationships: history, meta-analysis and recommendations. J Appl Ichthyol 22(4):241–253. https://doi.org/10.1111/j.1439-0426.2006.00805.x
Guzmán-Osorio FJ, Domínguez-Rodríguez VI, Adams RH, Lobato-García CE, Guerrero-Peña A, Barajas-Hernández JR (2021) Classification of petroleum origin and integrity by FTIR. Egypt J Pet 30(2):63–67. https://doi.org/10.1016/j.ejpe.2021.03.003
Hansen BH, Sørensen L, Carvalho PA, Meier S, Booth AM, Altin D, Nordtug T (2018) Adhesion of mechanically and chemically dispersed crude oil droplets to eggs of Atlantic cod (Gadus morhua) and haddock (Melanogrammus aeglefinus). Sci Total Environ 640:138–143. https://doi.org/10.1016/j.scitotenv.2018.05.207
Hassell KL, Coutin PC, Nugegoda D (2008) Hypoxia impairs embryo development and survival in black bream (Acanthopagrus butcheri). Mar Pollut Bull 57:302–306. https://doi.org/10.1016/j.marpolbul.2008.02.045
Hatlen K, Sloan CA, Burrows DG, Collier TK, Sholtz NL, Incardona JP (2010) Natural sunlight and residual fuel oils are an acutely lethal combination for fish embryos. Aquat Toxicol 99(1):56–64. https://doi.org/10.1016/j.aquatox.2010.04.002
Heintz RA, Rice SD, Wertheimer AC, Bradshaw RF, Thrower FP, Joyce JE, Short JW (2000) Delayed effects on growth and marine survival of pink salmon Oncorhynchus gorbuscha after exposure to crude oil during embryonic development. Mar Ecol Prog Ser 208:205–216. https://doi.org/10.3354/meps208205
Hicken CE, Linbo TL, Baldwin DH, Willis ML, Myers MS, Holland L, Incardona JP (2011) Sublethal exposure to crude oil during embryonic development alters cardiac morphology and reduces aerobic capacity in adult fish. PNAS 108(17):7086–7090. https://doi.org/10.1073/pnas.1019031108
Hodson PV (2017) The toxicity to fish embryos of PAH in crude and refined oils. Arch Environ Contam Toxicol 73(1):12–18. https://doi.org/10.1007/s00244-016-0357-6
Incardona JP, Scholz NL (2016) The influence of heart developmental anatomy on cardiotoxicity-based adverse outcome pathways in fish. Aquat Toxicol 177:515–525. https://doi.org/10.1016/j.aquatox.2016.06.016
Incardona JP, Collier TK, Scholz NL (2004) Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicol Appl Pharmacol 196(2):191–205. https://doi.org/10.1016/j.taap.2003.11.026
Incardona JP, Day HL, Collier TK, Scholz NL (2006) Developmental toxicity of 4-ring polycyclic aromatic hydrocarbons in zebrafish is differentially dependent on AH receptor isoforms and hepatic cytochrome P4501A metabolism. Toxicol Appl Pharmacol 217(3):308–321
Incardona JP, Vines CA, Anulacion BF, Baldwin DH, Day HL, French BL, Sloan CA (2012) Unexpectedly high mortality in Pacific herring embryos exposed to the 2007 Cosco Busan oil spill in San Francisco Bay. PNAS 109(2):E51–E58. https://doi.org/10.1073/pnas.1108884109
Incardona JP, Swarts TL, Edmunds RC, Linbo TL, Aquilina-Beck A, Sloan CA, Scholz NL (2013) Exxon Valdez to Deepwater Horizon: comparable toxicity of both crude oils to fish early life stages. Aquat Toxicol 142–143:303–316. https://doi.org/10.1016/j.aquatox.2013.08.011
Incardona JP, Gardner LD, Linbo TL, Brown TL, Esbaugh AJ, Mager EM, Stieglitz JD, French BL, Labenia JS, Laetz CA, Tagal M, Sloan CA, Elizur A, Benetti DD, Grosell M, Block BA, Scholz NL (2014) Deepwater Horizon crude oil impacts the developing hearts of large predatory pelagic fish. Proc Natl Acad Sci 111(15):E1510–E1518
International Organization for Standardization (2002) Water quality - Determination of 15 polycyclic aromatic hydrocarbons (PAH) in water. ISO 17993:2002, Geneva
International Organization for Standardization (2003) Water quality - determination of 15 polycyclic aromatic hydrocarbons (PAH) in water. ISO 17993:2003, Geneva
Johann S, Nüßer L, Goßen M, Hollert H, Seiler TB (2020) Differences in biomarker and behavioral responses to native and chemically dispersed crude and refined fossil oils in zebrafish early life stages. Sci Total Environ 709:136174. https://doi.org/10.1016/j.scitotenv.2019.136174
Johansen JL, Allan BJM, Rummer JL, Esbaugh AJ (2017) Oil exposure disrupts early life-history stages of coral reef fishes via behavioural impairments. Nat Ecol Evol 1:1146–1152. https://doi.org/10.1038/s41559-017-0232-5
Jung JH, Hicken CE, Boyd D, Anulacion BF, Carls MG, Shim WJ, Incardona JP (2013) Geologically distinct crude oils cause a common cardiotoxicity syndrome in developing zebrafish. Chemosphere 91(8):1146–1155. https://doi.org/10.1016/j.chemosphere.2013.01.019
Khursigara AJ, Perrichon P, Martinez-Bautista N, Burggren WW, Esbaugh AJ (2017) Cardiac function and survival are affected by crude oil in larval red drum, Sciaenops ocellatus. Sci Total Environ 579:797–804. https://doi.org/10.1016/j.scitotenv.2016.11.026
Laurel BJ, Copeman LA, Iseri P, Spencer ML, Hutchinson G, Nordtug T, Donald CE, Meier S, Allan SE, Boyd DT, Ylitalo GM, Cameron JR, French BL, Linbo TL, Scholz NL, Incardona P (2019) Embryonic crude oil exposure impairs growth and lipid allocation in a keystone Artic forage fish. iScience 19: 1101-1113. https://doi.org/10.1016/j.isci.2019.08.051
Li X, Ding G, Xiong Y, Ma X, Fan Y, Xiong D (2018) Toxicity of water-accommodated fractions (WAF), chemically enhanced WAF (CEWAF) of Oman crude oil and dispersant to early-life stages of zebrafish (Danio rerio). B Environ Contam Toxicol 101(3):314–319. https://doi.org/10.1007/s00128-018-2413-6
Ma Z, Sun Q, Ye J, Yao Q, Zhao C (2016) Study on the thermal degradation behaviors and kinetics of alkali lignin for production of phenolic-rich bio-oil using TGA-FTIR and Py- GC/MS. JAAP 117:116–124
Mager EM, Pasparakis C, Schlenker LS, Yao Z, Bodinier C, Stieglitz JD, Hoenig R, Morris JM, Benetti DD, Grosell M (2017) Assessment of early life stage mahi-mahi windows of sensitivity during acute exposures to Deepwater Horizon crude oil. Environ Toxicol Chem 36(7):1887–1895. https://doi.org/10.1002/etc.3713
Márquez-Couturier G, Vazquez-Navarrete CJ, Contreras-Sanchez WM, Álvarez-González CA (2015) Acuicultura Tropical Sustentable: Una estrategia para la producción y conservación del pejelagarto (Atractosteus tropicus) en Tabasco, México. Universidad Juárez Autónoma de Tabasco, Villahermosa
Martínez-Bautista G, Peña E, Martínez R, Camarillo S, Burggren W, Álvarez-González CA (2021) Survival, growth, and development in the early stages of the tropical gar Atractosteus tropicus: developmental critical windows and the influence of temperature, salinity, and oxygen availability. Fishes 6:5. https://doi.org/10.3390/fishes6010005
Mason JC (1969) Hypoxial stress prior to emergence and competition among coho salmon fry. J Fish Res Board Can 26:63–91. https://doi.org/10.1139/f69-007
Masood S, Saeed R, Ali M, Bagum S, Ashfaq M, Khan SR (2017) FTIR and thermodynamic study of Pakistani and international crude oils in 1,4-dioxane. Pet Sci Technol 35(8):754–760. https://doi.org/10.1080/10916466.2016.1273243
Meador JP, Nahrgang J (2019) Characterizing crude oil toxicity to early-life stage fish based on a complex mixture: are we making unsupported assumptions? Environ Sci Technol 53(19):11080–11092. https://doi.org/10.1021/acs.est.9b02889
Miller RR, Minckley WL, Norris SM, Schmitter Soto JJ (2009) Freshwater fishes of Mexico. University of Chicago Press, Chicago. https://doi.org/10.1086/509452?journalCode=qrb
Mora-Jamett M, Cabrera-Peña J, Galeano G (1997) Reproducción y alimentación del gaspar Atractosteus tropicus (Pisces: Lepisosteidae) en el refugio nacional de vida Silvestre Caño Negro, Costa Rica. Rev Biol Trop 45(2):861–866 https://revistas.ucr.ac.cr/index.php/rbt/article/view/20891
Morris JM, Gielazyn M, Krasnec MO, Takeshita R, Forth HP, Labenia JS, Scholz NL (2018) Crude oil cardiotoxicity to red drum embryos is independent of oil dispersion energy. Chemosphere 213:205–214. https://doi.org/10.1016/j.chemosphere.2018.09.015
Nahrgang J, Bender ML, Meier S, Nechev J, Berge J, Frantzen M (2019) Growth and metabolism of adult polar cod (Boreogadus saida) in response to dietary crude oil. Ecotox Environ Saf 180:53–62. https://doi.org/10.1046/j.1467-2979.2003.00120.x
Nelson D, Stieglitz JD, Cox GK, Heuer RM, Benetti DD, Grosell M, Crossley DA II (2017) Cardio-respiratory function during exercise in the cobia, Rachycentron canadum: The impact of crude oil exposure. Comp Biochem Physiol 201C:58–65. https://doi.org/10.1016/j.cbpc.2017.08.006
Olsen E, Aanes S, Mehl S, Holst JC, Aglen A, Gjosaeter H (2010) Cod, haddock, saithe, herring, and capelin in the Barents Sea and adjacent waters: a review of the biological value of the area. ICES J Mar Sci 67:87–101. https://doi.org/10.1093/icesjms/fsp229
Pasparakis C, Mager EM, Stieglitz JD, Benetti D, Grosell M (2016) Effects of Deepwater Horizon crude oil exposure, temperature and developmental stage on oxygen consumption of embryonic and larval mahi-mahi (Coryphaena hippurus). Aquat Toxicol 181:113–123. https://doi.org/10.1016/j.aquatox2016.10.022
Pasparakis C, Esbaugh AJ, Burggren W, Grosell M (2019) Physiological impacts of Deepwater Horizon oil on fish. Comp Biochem Physiol 224C:108558. https://doi.org/10.1016/j.cbpc.2019.06.002
Pelster B, Gittenberger-de Groot AC, Poelmann RE, Rombough P, Schwerte T, Thompson MB (2010) Functional plasticity of the developing cardiovascular system: examples from different vertebrates. Physiol Biochem Zool 83:775–791. https://doi.org/10.1086/656004
Pepin P (1991) Effect of temperature and size on development, mortality, and survival rates of the pelagic early life history stages of marine fish. Can J Fish Aquat Sci 48:503–518. https://doi.org/10.1139/f91-065
Perrichon P, Le Menach K, Akcha F, Cachot J, Budzinski H, Bustamante P (2016) Toxicity assessment of water-accommodated fractions from two different oils using a zebrafish (Danio rerio) embryo-larval bioassay with a multilevel approach. Sci Total Environ 568:952–966. https://doi.org/10.1016/j.scitotenv.2016.04.186
Perrichon P, Grosell M, Burggren W (2017) Heart performance determination by visualization in larval fishes: influence of alternative models for heart shape and volume. Front Physiol 8:464. https://doi.org/10.3389/fphys.2017.00464
Perrichon P, Mager EM, Pasparakis C, Stieglitz JD, Benetti DD, Grosell M, Burggren WW (2018) Combined effects of elevated temperature and Deepwater Horizon oil exposure on the cardiac performance of larval mahi-mahi, Coryphaena hippurus. PLoS One 13(10):e0203949. https://doi.org/10.1371/journal.pone.0203949
Raimondo S, Jackson CR, Krzykwa J, Hemmer BL, Awkerman JA, Barron MG (2014) Developmental toxicity of Louisiana crude oil-spiked sediment to zebrafish. Ecotox Environ Saf 108:265–272. https://doi.org/10.1016/j.ecoenv.2014.07.020
Raimondo S, Hemmer BL, Lilavois CR, Krzykwa J, Almario A, Awkerman JA, Barron MG (2016) Effects of Louisiana crude oil on the sheepshead minnow (Cyprinodon variegatus) during a life-cycle exposure to laboratory oiled sediment. Environ Toxicol 31(11):1627–1639. https://doi.org/10.1002/tox.22167
Rakhmatullin IZ, Efimov SV, Tyurin VA, Al-Muntaser AA, Klimovitskii AE, Varfolomeev MA, Klochkov VV (2018) Application of high resolution NMR (1H and13C) and FTIR spectroscopy for characterization of light and heavy crude oils. J Pet Sci Eng 168:256–262. https://doi.org/10.1016/j.petrol.2018.05.011
Reséndez AM (1981) Estudio de los peces de la Laguna de Términos, Campeche, México. II. Última parte. Biótica 6(3): 239–291
Reséndez-Medina A, Salvadores ML (1983) Contribución al conocimiento de la biología del pejelagarto Lepisosteus tropicus (Gill) y la tenguayaca Petenia splendida Günther, del estado de Tabasco. Biotica 8:413–426 https://eurekamag.com/research/020/774/020774436.php
Rodgers ML, Jones ER, Klinkhamer C, Mahapatra CT, Serafin J, Bosker T, Sepúlveda MS (2018) Combined effects of Deepwater Horizon crude oil and environmental stressors on Fundulus grandis embryos. Environ Toxicol Chem 37(7):1916–1925. https://doi.org/10.1002/etc.4153
Rudneva I (2013) Biomarkers for stress in fish embryos and larvae. CRC Press, Boca Raton. https://doi.org/10.1201/b15378
Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68(4):369–392. https://doi.org/10.1016/j.aquatox.2004.03.016
Sloan CA, Brown DW, Pearce RW, Boyer RH, Bolton JL, Burrows DG, Herman DP, Krahn MM (2005) Determining aromatic hydrocarbons and chlorinated hydrocarbons in sediments and tissues using accelerated solvent extraction and gas chromatography/mass spectrometry. In: Ostrander GK (ed) In. Techniques in Aquatic Toxicology, 2nd edn. CRC Press, Boca Raton, pp 631–651. https://doi.org/10.1201/9780203501597.CH35
Sørensen L, Sørhus E, Nordtug T, Incardona JP, Linbo TL, Giovanetti L, Meier S (2017) Oil droplet fouling and differential toxicokinetics of polycyclic aromatic hydrocarbons in embryos of Atlantic haddock and cod. PLoS One 12(7):e0180048. https://doi.org/10.1371/journal.pone.0180048
Sørhus E, Edvardsen RB, Karlsen Ø, Nordtug T, van der Meeren T, Thorsen A, Meier S (2015) Unexpected interaction with dispersed crude oil droplets drives severe toxicity in Atlantic haddock embryos. PLoS One 10(4):e0124376. https://doi.org/10.1371/journal.pone.0124376
Tuomisto JT, Asikainen A, Meriläinen P, Haapasaari P (2020) Health effects of nutrients and environmental pollutants in Baltic herring and salmon: a quantitative benefit-risk assessment. BMC Public Health 20(1):64. https://doi.org/10.1186/s12889-019-8094-1
Weis P, Weis JS (1974) Cardiac-malformation and other effects due to insecticides in embryos of killifish, Fundulus heteroclitus. Teratology 10:263–267. https://doi.org/10.1002/tera.1420100308
Weis P, Weis JS (1977) Methylmercury teratogenesis in killifish, Fundulus heteroclitus. Teratology 16:317–325. https://doi.org/10.1002/tera.1420160311
Yang L, Ho NY, Alshut R, Legradi J, Weiss C, Reischl M, Mikut R, Liebel U, Mueller F, Straehle U (2009) Zebrafish embryos as models for embryotoxic and teratological effects of chemicals. Reprod Toxicol 28:245–253. https://doi.org/10.1016/j.reprotox.2009.04.013
Acknowledgements
We thank the National Council of Science and Technology in Mexico for the scholarship for Simrith Elizabeth Córdova de la Cruz and the Remediation Laboratory if the Universidad Juárez Autónoma de Tabasco for providing the crude oil samples for this study.
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Gabriel Núñez-Nogueira received support from the Programa Institucional para la Incorporación al Sistema Nacional de Investigadores UJAT Program.
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SECC performed the experiments for her master thesis, analyzed data, interpreted results of experiments, prepared figures and tables, and drafted this manuscript. CAAG and WWB were the advisers of the master thesis, contributed to the conception and design of this research, and edited and approved the final manuscript. GMB, GNN, ESPM, RMG, and RHA contributed with the material preparation, data collection, and data analysis, edited previous versions of the manuscript, and approved the final manuscript.
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Córdova-de la Cruz, S.E., Martínez-Bautista, G., Peña-Marín, E.S. et al. Morphological and cardiac alterations after crude oil exposure in the early-life stages of the tropical gar (Atractosteus tropicus). Environ Sci Pollut Res 29, 22281–22292 (2022). https://doi.org/10.1007/s11356-021-17208-9
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DOI: https://doi.org/10.1007/s11356-021-17208-9