Share This Article:

Deepwater Horizon Oil Spill as a Case Study for Interdisciplinary Cooperation within Developmental Biology, Environmental Sciences and Physiology

Full-Text HTML XML Download Download as PDF (Size:903KB) PP. 7-23
DOI: 10.4236/wjet.2015.34C002    3,294 Downloads   3,725 Views   Citations


The Deepwater Horizon Oil Spill in the USA’s Gulf of Mexico created a high degree of exposure of marine organisms to toxic polyaromatic hydrocarbons (PAHs) present in crude oil. To determine the ecological and physiological effects of crude oil on the Gulf of Mexico ecosystem, the Gulf of Mexico Research Initiative created several research consortia to address overreaching questions concerning the biological impacts of the ecology of the Gulf of Mexico that would otherwise be beyond the capabilities of an individual investigator or a small group. One of these consortia, highlighted in this article, is the RECOVER Consortium, which brings together physiologists, developmental biologists, toxicologists and other life scientists to focus on the multifaceted physiological effects of PAHs, especially as they pertain to cardiovascular and metabolic physiology of economically important fish species. Using the Recover Consortium’s interdisciplinary approach to revealing the biological impacts of the Deepwater Horizon Oil Spill as a case study, we make the argument for interdisciplinary teams that bring together scientists with different specialties as an efficient way—and perhaps the only way—to unravel highly complex biological effects of marine oil spills.

Cite this paper

Burggren, W. , Dubansky, B. , Roberts, A. and Alloy, M. (2015) Deepwater Horizon Oil Spill as a Case Study for Interdisciplinary Cooperation within Developmental Biology, Environmental Sciences and Physiology. World Journal of Engineering and Technology, 3, 7-23. doi: 10.4236/wjet.2015.34C002.


[1] Spies, R.B., et al. (1996) Biomarkers of Hydrocarbon Exposure and Sublethal Effects in Embiotocid Fishes from a Natural Petroleum Seep in the Santa Barbara Channel. Aquatic Toxicology, 34, 195-219.
[2] Jernelov, A. (2010) The Threats from Oil Spills: Now, Then, and in the Future. Ambio, 39, 353-366.
[3] Turner, R.E., et al. (2014) Distribution and Recovery Trajectory of Macondo (Mississippi Canyon 252) Oil in Louisiana Coastal Wetlands. Marine Pollution Bulletin, 87, 57-67.
[4] McNutt, M.K., et al. (2012) Applications of Science and Engineering to Quantify and Control the Deepwater Horizon Oil Spill. Proceedings of the National Academy of Sciences of the United States of America, 109, 20222-20228.
[5] McNutt, M.K., et al. (2012) Review of Flow Rate Estimates of the Deepwater Horizon Oil Spill. Proceedings of the National Academy of Sciences of the United States of America, 109, 20260-20267.
[6] Liu, Z., Liu, J., Zhu, Q. and Wu, W. (2012) The Weathering of Oil after the Deepwater Horizon Oil Spill: Insights from the Chemical Composition of the Oil from the Sea Surface, Salt Marshes and Sediments. Environmental Research Letters, 7, 14.
[7] Ball, A. and ruskewycz, A. (2013) Polyaromatic Hydrocarbon Exposure: An Ecological Impact Ambiguity. Environmental Science and Pollution Research, 20, 4311-4326.
[8] Tuvikene, A. (1995) Responses of Fish to Polycyclic Aromatic-Hydrocarbons (PAHs). Annales Zoologici Fennici, 32, 295-309.
[9] Pennings, S.C., McCall, B.D. and Hooper-Bui, L. (2014) Effects of Oil Spills on Terrestrial Arthropods in Coastal Wetlands. Bioscience, 64, 789-795.
[10] Klingbeil, E.C., et al. (2014) Polycyclic Aromatic Hydrocarbons, Tobacco Smoke, and Epigenetic Remodeling in Asthma. Immunologic Research, 58, 369-373.
[11] Heintz, R.A., et al. (2000) Delayed Effects on Growth and Marine Survival of Pink Salmon (Oncorhynchus gorbuscha) after Exposure to Crude Oil during Embryonic Development. Marine Ecology-Progress Series, 208, 205-216.
[12] Kolian, S.R., et al. (2015) Oil in the Gulf of Mexico after the Capping of the BP/Deepwater Horizon Mississippi Canyon (MC-252) Well. Environmental Science and Pollution Research, 22, 12073-12082.
[13] Turner, R.E., et al. (2014) Changes in the Concentration and Relative Abundance of Alkanes and PAHs from the Deepwater Horizon Oiling of Coastal Marshes. Marine Pollution Bulletin, 86, 291-297.
[14] Lin, Q. and Mendelssohn, I.A. (2012) Impacts and Recovery of the Deepwater Horizon Oil Spill on Vegetation Structure and Function of Coastal Salt Marshes in the Northern Gulf of Mexico. Environmental Science & Technology, 46, 3737-3743.
[15] Pilcher, W., et al. (2014) Genomic and Genotoxic Responses to Controlled Weathered-Oil Exposures Confirm and Extend Field Studies on Impacts of the Deepwater Horizon Oil Spill on Native Killifish. PLoS ONE, 9, 11.
[16] Rousselet, E., et al. (2013) Evaluation of Immune Functions in Captive Immature Loggerhead Sea Turtles (Caretta caretta). Veterinary Immunology and Immunopathology, 156, 43-53.
[17] Yu, S.Y., Halbrook, R.S. and Sparling, D.W. (2012) Accumulation of Polychlorinated Biphenyls (PCBs) and Evaluation of Hematological and Immunological Effects of PCB Exposure on Turtles. Bulletin of Environmental Contamination and Toxicology, 88, 823-827.
[18] Dubansky, B., et al. (2013) Multi-Tissue Molecular, Genomic, and Developmental Effects of the Deepwater Horizon Oil Spill on Resident Gulf Killifish (Fundulus grandis). Environ. Sci. Technol., 47, 5074-5082.
[19] Barron, M.G. (2012) Ecological Impacts of the Deepwater Horizon Oil Spill: Implications for Immunotoxicity. Toxicologic Pathology, 40, 315-320.
[20] Kim, S., Sundaramoorthi, H. and Jagadeeswaran, P. (2015) Dioxin-Induced Thrombocyte Aggregation in Zebrafish. Blood Cells Mol Dis, 54, 116-122.
[21] Incardona, J.P., et al. (2014) Deepwater Horizon Crude Oil Impacts the Developing Hearts of Large Predatory Pelagic fish. Proceedings of the National Academy of Sciences of the United States of America, 111, E1510-E1518.
[22] Mager, E.M., et al. (2014) Acute Embryonic or Juvenile Exposure to Deepwater Horizon Crude Oil Impairs the Swimming Performance of Mahi-Mahi (Coryphaena hippurus). Environmental Science & Technology, 48, 7053-7061.
[23] McMillan, B.J. and Bradfield, C.A. (2007) The Aryl Hydrocarbon Receptor Sans Xenobiotics: Endogenous Function in Genetic Model Systems. Molecular Pharmacology, 72, 487-498.
[24] Okey, A.B. (2007) An Aryl Hydrocarbon Receptor Odyssey to the Shores of Toxicology: The Deichmann Lecture, International Congress of Toxicology-XI. Toxicological Sciences, 98, 5-38.
[25] Beischlag, T.V., et al. (2008) The Aryl Hydrocarbon Receptor Complex and the Control of Gene Expression. Crit Rev Eukaryot Gene Expr, 18, 207-50.
[26] Oziolor, E.M., et al. (2014) Evolved Resistance to PCB- and PAH-Induced Cardiac Teratogenesis, and Reduced CYP1A Activity in Gulf Killifish (Fundulus grandis) Populations from the Houston Ship Channel, Texas. Aquat Toxicol, 150, 210-219.
[27] Stephens, S.M., et al. (2000) Sub-Lethal Effects of Exposure of Juvenile Turbot to Oil Produced Water. Marine Pollution Bulletin, 40, 928-937.
[28] Whitehead, A., et al. (2012) Genomic and Physiological Footprint of the Deepwater Horizon Oil Spill on Resident Marsh Fishes. Proc. Natl. Acad. Sci., 109, 20298-20302.
[29] Hicken, C.E., et al. (2011) Sublethal Exposure to Crude Oil during Embryonic Development Alters Cardiac Morphology and Reduces Aerobic Capacity in Adult Fish. Proceedings of the National Academy of Sciences of the United States of America, 108, 7086-7090.
[30] Browne, M.A., et al. (2015) Linking Effects of Anthropogenic Debris to Ecological Impacts. Proceedings of the Royal Society B-Biological Sciences, 282, 10.
[31] Whitehead, A. (2013) Interactions between Oil-Spill Pollutants and Natural Stressors Can Compound Ecotoxicological Effects. Integr Comp Biol, 53, 635-47.
[32] McBryan, T.L., et al. (2013) Responses to Temperature and Hypoxia as Interacting Stressors in Fish: Implications for Adaptation to Environmental Change. Integrative and Comparative Biology, 53, 648-659.
[33] Whitehead, A., et al. (2012) Salinity- and Population-Dependent Genome Regulatory Response during Osmotic Acclimation in the Killifish (Fundulus heteroclitus) Gill. Journal of Experimental Biology, 215, 1293-1305.
[34] Whitehead, A., et al. (2012) Common Mechanism Underlies Repeated Evolution of Extreme Pollution Tolerance. Proceedings of the Royal Society B: Biological Sciences, 279, 427-433.
[35] Wirgin, I. and Waldman, J.R. (2004) Resistance to Contaminants in North American Fish Populations. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 552, 73-100.
[36] Oziolor, E.M., Dubansky, B. and Matson, C.W. (2016) Fitness Costs and Cross-Resistance in Gulf Killifish (Fundulus grandis) Populations, Resistant to Chronic PCB and PAH Contamination in the Houston Ship Channel, Texas. Aquat Toxicol, (Submitted).
[37] Brette, F., et al. (2014) Crude Oil Impairs Cardiac Excitation-Contraction Coupling in Fish. Science, 343, 772-776.
[38] Incardona, J.P., Collier, T.K. and Scholz, N.L. (2011) Oil Spills and Fish Health: Exposing the Heart of the Matter. Journal of Exposure Science and Environmental Epidemiology, 21, 3-4.
[39] Rabalais, N.N., Turner, R.E. and Wiseman, W.J. (2002) Gulf of Mexico Hypoxia, Aka “The Dead Zone”. Annual Review of Ecology and Systematics, 33, 235-263.
[40] Lindsey, S. and Papoutsakis, E.T. (2012) The Evolving Role of the Aryl Hydrocarbon Receptor (AHR) in the Normophysiology of Hematopoiesis. Stem Cell Reviews and Reports, 8, 1223-1235.
[41] Vorrink, S.U., et al. (2014) Hypoxia Perturbs Aryl Hydrocarbon Receptor Signaling and CYP1A1 Expression Induced by PCB 126 in Human Skin and Liver-Derived Cell Lines. Toxicology and Applied Pharmacology, 274, 408-416.
[42] Thomas, P. and Rahman, M.S. (2012) Extensive Reproductive Disruption, Ovarian Masculinization and Aromatase Suppression in Atlantic Croaker in the Northern Gulf of Mexico Hypoxic Zone. Proceedings of the Royal Society B-Biological Sciences, 279, 28-38.
[43] Ahmad, Z., et al. (2003) Seasonal Variation of UV Radiation in the Ocean under Clear and Cloudy Conditions.
[44] Tedetti, M. and Sempéré, R. (2006) Penetration of Ultraviolet Radiation in the Marine Environment. A Review. Photochemistry and Photobiology, 82, 389-397.
[45] Fischer, J.M., et al. (2006) Effects of Ultraviolet Radiation on Diel Vertical Migration of Crustacean Zooplankton: An in Situ Mesocosm Experiment. Hydrobiologia, 563, 217-224.
[46] Gevertz, A.K., et al. (2012) Differential Tolerance of Native and Nonnative Fish Exposed to Ultraviolet Radiation and Fluoranthene in Lake Tahoe (California/Nevada), USA. Environmental Toxicology and Chemistry, 31, 1129-1135.
[47] Leech, D.M. and Williamson, C.E. (2001) In Situ Exposure to Ultraviolet Radiation Alters the Depth Distribution of Daphnia. Limnology and Oceanography, 46, 416-420.
[48] Moeller, R.E., et al. (2005) Dietary Acquisition of Photoprotective Compounds (Mycosporine-Like Amino Acids, Carotenoids) and Acclimation to Ultraviolet Radiation in a Freshwater Copepod. Limnology and Oceanography, 50, 427- 439.
[49] Persaud, A.D., et al. (2007) Photoprotective Compounds in Weakly and Strongly Pigmented Copepods and Co-Occur- ring Cladocerans. Freshwater Biology, 52, 2121-2133.
[50] Diamond, S.A. (2003) Photoactivated Toxicity in Aquatic Environments. In: Uv Effects in Aquatic Organisms and Ecosystems, 219.
[51] McCloskey, J.T. and Oris, J.T. (1993) Effect of Anthracene and Solar Ultraviolet Radiation Exposure on Gill ATPase and Selected Hematologic Measurements in the Bluegill Sunfish (Lepomis macrochirus). Aquatic Toxicology (Amsterdam), 24, 207-217.
[52] Weinstein, J.E., Oris, J.T. and Taylor, D.H. (1997) An Ultrastructural Examination of the Mode of UV-Induced Toxic Action of Fluoranthene in the Fathead Minnow, Pimephales promelas. Aquatic Toxicology, 39, 1-22.
[53] Arfsten, D.P., Schaeffer, D.J. and Mulveny, D.C. (1996) The Effects of Near Ultraviolet Radiation on the Toxic Effects of Polycyclic Aromatic Hydrocarbons in Animals and Plants: A Review. Ecotoxicology and Environmental Safety, 33, 1-24.
[54] Holst, L.L. and Giesy, J.P. (1989) Chronic Effects of the Photoenhanced Toxicity of Anthracene on Daphnia-Magna Reproduction. Environmental Toxicology and Chemistry, 8, 933-942.
[55] Hatch, A.C. and Burton Jr., G.A. (1999) Photo-Induced Toxicity of PAHs to Hyalella azteca and Chironomus tentans: Effects of Mixtures and Behavior. Environmental Pollution, 106, 157-167.
[56] Oris, J.T. and Giesy, J.P. (1986) Photoinduced Toxicity of Anthracene to Juvenile Bluegill Sunfish (Lepomis Macrochirus Rafinesque): Photoperiod Effects and Predictive Hazard Evaluation. Environmental Toxicology and Chemistry, 5, 761-768.
[57] Hatch, A. and Burton Jr., G.A. (1999) Phototoxicity of Fluoranthene to Two Freshwater Crustaceans, Hyalella azteca and Daphnia magna: Measures of Feeding Inhibition as a Toxicological Endpoint. Hydrobiologia, 400, 243-248.
[58] Cooke, S.L., Williamson, C.E. and Saros, J.E. (2006) How Do Temperature, Dissolved Organic Matter and Nutrients Influence the Response of Leptodiaptomus ashlandi to UV Radiation in a Subalpine Lake? Freshwater Biology, 51, 1827-1837.
[59] Williamson, C.E., et al. (1996) Ultraviolet Radiation in North American Lakes: Attenuation Estimates from DOC Measurements and Implications for Plankton Communities. Limnology and Oceanography, 41, 1024-1034.
[60] Weinstein, J.E. (2003) Influence of Salinity on the Bioaccumulation and Photoinduced Toxicity of Fluoranthene to an Estuarine Shrimp and Oligochaete. Environmental Toxicology and Chemistry, 22, 2932-2939.
[61] Alloy, M.M., et al. (2015) Photo-Induced Toxicity of Deepwater Horizon Slick oil to Blue Crab (Callinectes sapidus) Larvae. Environmental Toxicology and Chemistry, 34, 2061-2066.
[62] Haney, J.C., Geiger, H.J. and Short, J.W. (2014) Bird Mortality From the Deepwater Horizon Oil Spill. II. Carcass Sampling and Exposure Probability in the Coastal Gulf of Mexico. Marine Ecology Progress Series, 513, 239-252.
[63] Haney, J.C., Geiger, H.J. and Short, J.W. (2014) Bird Mortality from the Deepwater Horizon Oil Spill. I. Exposure Probability in the Offshore Gulf of Mexico. Marine Ecology Progress Series, 513, 225-237.
[64] Finch, B.E., et al. (2012) Embryotoxicity of Mixtures of Weathered Crude Oil Collected from the Gulf of Mexico and Corexit 9500 in Mallard Ducks (Anas platyrhynchos). Science of the Total Environment, 426, 155-159.
[65] Wooten, K.J., Finch, B.E. and Smith, P.N. (2012) Embryotoxicity of Corexit 9500 in Mallard Ducks (Anas platyrhynchos). Ecotoxicology, 21, 662-666.
[66] Finch, B.E., Wooten, K.J. and Smith, P.N. (2011) Embryotoxicity of Weathered Crude Oil from the Gulf of Mexico in Mallard Ducks (Anas Platyrhynchos). Environmental Toxicology and Chemistry, 30, 1885-1891.
[67] Albers, P.H. (1978) The Effects of Petroleum of Different Stages of Incubation in Bird Eggs. Bull Environ Contam Toxicol, 19, 624-30.
[68] Darwin, C. (1859) On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. W. Clowes and Sons, London, 491.
[69] Dubansky, B., et al. (2014) Response to Comment on “Multi-Tissue Molecular, Genomic, and Developmental Effects of the Deepwater Horizon Oil Spill on Resident Gulf Killifish (Fundulus grandis)”. Environmental Science & Technology.
[70] Pearson, W.H. (2014) Comment on “Multitissue Molecular, Genomic, and Developmental Effects of the Deepwater Horizon Oil Spill on Resident Gulf Killifish (Fundulus grandis)”. Environmental Science & Technology.
[71] Incardona, J.P., et al. (2013) Exxon Valdez to Deepwater Horizon: Comparable Toxicity of both Crude Oils to Fish Early Life Stages. Aquatic Toxicology, 142, 303-316.
[72] Fodrie, F.J., et al. (2014) Integrating Organismal and Population Responses of Estuarine Fishes in Macondo Spill Research. Bioscience, 64, 778-788.
[73] Colwell, R.R. (2014) Understanding the Effects of the Deepwater Horizon Oil Spill. Bioscience, 64, 755-755.
[74] Burggren, W.W. and Mueller, C.A. (2014) A 3-D, System Approach for Developmental Critical Windows. Physiological Biochemistry and Zoology, in Press.
[75] Burggren, W.W. (1998) Studying Physiological Development: Past, Present and Future. Biological Bulletin of the National Taiwan Normal University, 33, 71-84.
[76] Burggren, W.W. and Reyna, K.S. (2011) Developmental Trajectories, Critical Windows and Phenotypic Alteration during Cardio-Respiratory Development. Respir Physiol Neurobiol, 178, 13-21.
[77] Rice, D. and Barone, Jr., S. (2000) Critical Periods of Vulnerability for the Developing Nervous System: Evidence from Humans and Animal Models. Environ Health Perspect, 108, 511-533.
[78] Nijland, M.J., Ford, S.P. and Nathanielsz, P.W. (2008) Prenatal Origins of adult Disease. Curr Opin Obstet Gynecol, 20, 132-138.
[79] Loebrich, S. and Nedivi, E. (2009) The Function of Activity-Regulated Genes in the Nervous System. Physiol Rev, 89, 1079-1103.
[80] Hensch, T.K. and Bilimoria, P.M. (2012) Re-Opening Windows: Manipulating Critical Periods for Brain Development. Cerebrum, 2012, 11.
[81] Robertson, C.E., et al. (2014) Hypoxia-Inducible Factor-1 Mediates Adaptive Developmental Plasticity of Hypoxia Tolerance in Zebrafish, Danio rerio. Proc Biol Sci, 281.
[82] Staaterman, E., Paris, C.B. and Helgers, J. (2012) Orientation Behavior in Fish Larvae: A Missing Piece to Hjort’s Critical Period Hypothesis. Journal of Theoretical Biology, 304, 188-196.
[83] Gonzalez-Doncel, M., et al. (2005) Stage-Specific Toxicity of Cypermethrin to Medaka (Oryzias latipes) Eggs and Embryos Using a Refined Methodology for an in Vitro Fertilization Bioassay. Arch Environ Contam Toxicol, 48, 87-98.
[84] Burggren, W. and Blank, T. (2009) Physiological Study of Larval Fishes: Challenges and Opportunities. Scientia Marina, 2009, 99-110.
[85] Baccarelli, A. and Bollati, V. (2009) Epigenetics and Environmental Chemicals. Curr Opin Pediatr, 21, 243-251.
[86] Burggren, W. and Fritsche, R. (1995) Cardiovascular Measurements in Animals in the Milligram Range. Braz J Med Biol Res, 28, 1291-305.
[87] Pelster, B. and Burggren, W.W. (1996) Disruption of Hemoglobin Oxygen Transport Does Not Impact Oxygen-De- pendent Physiological Processes in Developing Embryos of Zebra Fish (Danio rerio). Circ Res, 79, 358-362.
[88] Burggren, W.W. (2000) Developmental Physiology, Animal Models, and the August Krogh Principle. Zoology-Analysis of Complex Systems, 102, 148-156.
[89] Bagatto, B. and Burggren, W. (2006) A Three-Dimensional Functional Assessment of Heart and Vessel Development in the Larva of the Zebrafish (Danio rerio). Physiol Biochem Zool, 79, 194-201.
[90] Grillitsch, S., et al. (2005) The Influence of Environmental P-O2 on Hemoglobin Oxygen Saturation in Developing Zebrafish Danio rerio. Journal of Experimental Biology, 208, 309-316.
[91] Egg, M., et al. (2014) Chronodisruption Increases Cardiovascular Risk in Zebrafish via Reduced Clearance of Senescent Erythrocytes. Chronobiol Int, 31, 680-689.
[92] Schwerte, T., Uberbacher, D. and Pelster, B. (2003) Non-Invasive Imaging of Blood Cell Concentration and Blood Distribution in Zebrafish Danio rerio Incubated in Hypoxic Conditions in Vivo. J Exp Biol, 206, 1299-1307.
[93] Cripe, G., et al. (2009) Multigenerational Exposure of the Estuarine Sheepshead Minnow (Cyprinodon variegatus) to 17 β-Estradiol. I. organism-Level Effects over Three Generations. Environ Toxicol Chem, 11, 2397-2408.
[94] Sutherland, J.E. and Costa, M. (2003) Epigenetics and the Environment. Ann N Y Acad Sci, 983,151-160.
[95] Bollati, V. and Baccarelli, A. (2010) Environmental Epigenetics. Heredity, 105, 105-112.
[96] Hala, D., Huggett, D.B., Burggren, W.W. (2014) Environmental Stressors and the Epigenome. Drug Discovery Today: Technologie, 12, e3-e8.
[97] Guerrero-Bosagna, C. and Skinner, M.K. (2014) Environmentally Induced Epigenetic Transgenerational Inheritance of Male Infertility. Curr Opin Genet Dev, 26, 79-88.
[98] Mirbahai, L. and Chipman, J.K. (2014) Epigenetic Memory of Environmental Organisms: A Reflection of Lifetime Stressor Exposures. Mutat Res Genet Toxicol Environ Mutagen, 764-765, 10-17.
[99] Klingbeil, E.C., et al. (2014) Polycyclic Aromatic Hydrocarbons, Tobacco Smoke, and Epigenetic Remodeling in Asthma. Immunol Res, 58, 369-373.
[100] Kim, M., et al. (2012) Environmental Toxicants—Induced Epigenetic Alterations and Their Reversers. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev, 30, 323-367.
[101] Perrichon, P., et al. (2015) Parental Trophic Exposure to Three Aromatic Fractions of Polycyclic Aromatic Hydrocarbons in the Zebrafish: Consequences for the Offspring. Sci Total Environ, 524-525, 52-62.
[102] Lyche, J.L., et al. (2013) Parental Exposure to Natural Mixtures of POPs Reduced Embryo Production and Altered Gene Transcription in Zebrafish Embryos. Aquat Toxicol, 126, 424-434.
[103] King Heiden, T.C., et al. (2009) Persistent Adverse Effects on Health and Reproduction Caused by Exposure of Zebrafish to 2,3,7,8-Tetrachlorodibenzo-p-dioxin during Early Development and Gonad Differentiation. Toxicological Sciences, 109, 75-87.
[104] Kong, R.Y., et al. (2008) Development of a Marine Fish Model for Studying in Vivo Molecular Responses in Ecotoxicology. Aquat Toxicol, 86, 131-141.
[105] Corrales, J., et al. (2014) Multigenerational Effects of Benzo[a]pyrene Exposure on Survival and Developmental Deformities in Zebrafish Larvae. Aquat Toxicol, 148, 16-26.
[106] Burggren, W.W. (2014) Epigenetics as a Source of Variation in Comparative Animal Physiology-or-Lamarck Is Lookin’ Pretty Good These Days. J Exp Biol, 217, 682-689.
[107] Burggren, W.W. (2015) Dynamics of Epigenetic Phenomena: Intergenerational and Intragenerational Phenotype “washout”. Journal of Experimental Biology, 218.
[108] Ho, D.H. and Burggren, W.W. (2012) Parental Hypoxic Exposure Confers Offspring Hypoxia Resistance in Zebrafish (Danio rerio). J Exp Biol, 215, 4208-4216.
[109] Burggren, W.W. and Crews, D. (2014) Epigenetics in Comparative Biology: Why We Should Pay Attention. Integrative and Comparative Biology, 54, 7-20.
[110] Burggren, W.W. (2015) Dynamics of Epigenetic Phenomena: Inter- and Intra-Generational Phenotype “Washout”. Journal of Experimental Biology, 218.
[111] Mager, E.M., et al. (2014) Acute Embryonic or Juvenile Exposure to Deepwater Horizon Crude Oil Impairs the Swimming Performance of Mahi-Mahi (Coryphaena hippurus). Environ Sci Technol, 48, 7053-7061.
[112] Watson, C.J., Nordi, W.M. and Esbaugh, A.J. (2014) Osmoregulation and Branchial Plasticity after Acute Freshwater Transfer in Red Drum, Sciaenops ocellatus. Comp Biochem Physiol A Mol Integr Physiol, 178, 82-89.
[113] Esbaugh, A.J., et al. (2015) Respiratory Plasticity Is Insufficient to Alleviate Blood Acid-Base Disturbances after Acclimation to Ocean Acidification in the Estuarine Red Drum, Sciaenops ocellatus. J Comp Physiol B.
[114] Roy, L.A., et al. (2003) Biochemical Effects of Petroleum Exposure in Hornyhead Turbot (Pleuronichthys verticalis) Exposed to a Gradient of Sediments Collected from a Natural Petroleum Seep in CA, USA. Aquat Toxicol, 65, 159-169.
[115] Andrewartha, S.J., Tazawa, H. and Burggren, W.W. (2011) Embryonic Control of Heart Rate: Examining Developmental Patterns and Temperature and Oxygenation Influences Using Embryonic avian Models. Respir Physiol Neurobiol, 178, 84-96.
[116] Burggren, W.W. and Warburton, S. (2007) Amphibians as Animal Models for Laboratory Research in Physiology. ILAR J, 48, 260-269.
[117] Walcott, B.P. and Peterson, R.T. (2014) Zebrafish Models of Cerebrovascular Disease. J Cereb Blood Flow Metab, 34, 571-577.
[118] Quaife, N.M., Watson, O. and Chico, T.J.A. (2012) Zebrafish: An Emerging Model of Vascular Development and Remodelling. Current Opinion in Pharmacology, 12, 608-614.
[119] Renshaw, S.A. and Trede, N.S. (2012) A Model 450 Million Years in the Making: Zebrafish and Vertebrate Immunity. Dis Model Mech, 5, 38-47.
[120] Krebs, H.A. (1975) The August Krogh Principle: “For Many Problems There Is an Animal on Which It Can Be Most Conveniently Studied”. J Exp Zool, 194, 221-226.
[121] Bennett, A.F. (2003) Experimental Evolution and the Krogh Principle: Generating Biological Novelty for Functional and Genetic Analyses. Physiol Biochem Zool, 76, 1-11.
[122] Mueller, C.A., Burggren, W. and Tazawa, H. (2014) The Physiology of the Avian Embryo. In: Whittow, G.C., Ed., Sturkie’s Avian Physiology, Elsivier, New York.
[123] Branum, S.R., Yamada-Fisher, M. and Burggren, W. (2013) Reduced Heart Rate and Cardiac Output Differentially Affect Angiogenesis, Growth, and Development in Early Chicken Embryos (Gallus domesticus). Physiol Biochem Zool, 86, 370-82.
[124] Burggren, W.W., et al. (2010) Interdisciplinarity in the Biological Sciences. In: R. Frodeman, R., Mitchum, C. and Hollbrook, J.B., Eds., Handbook of Interdisciplinarity, Oxford University Press, Oxford.

comments powered by Disqus

Copyright © 2017 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.