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Toxicity of petroleum hydrocarbons to Brachyuran crabs: a review of deleterious effects of oil-related xenobiotics on life stages

Published online by Cambridge University Press:  07 June 2021

Qusaie Karam  and
Zainab Al-Wazzan Open the ORCID record for Zainab Al-Wazzan [Opens in a new window]
Qusaie Karam
Affiliation:
Environment and Life Sciences Research Center, Kuwait Institute for Scientific Research, P.O. Box 24885, Safat13109, Kuwait
Zainab Al-Wazzan*
Affiliation:
Environment Protection Authority, P.O. Box 24395, Safat13104, Kuwait
*
Author for correspondence: Zainab Al-Wazzan, E-mail: zoology13@gmail.com
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Abstract

Petroleum hydrocarbons (PH) toxicity and bioaccumulation in aquatic organisms have been investigated for almost 50 years. Continuous oil spillages necessitate a further understanding of the toxicological effects of PH on brachyuran crabs. Crabs can be exposed to PH through various routes such as the water column, sediment and diet. Numerous investigations have been dedicated to evaluating PH toxicity on different life stages of crab species, but the majority of them have focused on the blue crab Callinectes sapidus as it represents an edible and favourable seafood commodity for human consumption. The objective of the review is to critically assess studies related to PH toxicity on different life stages of 41 crab species representing 13 families across the world. Several physiological, biochemical and genetic endpoints of marine crabs were evaluated in addition to the sublethal effects of PH on crab metabolism, behaviour, moulting, growth and survival. A concise summary of PH deleterious effects on different taxonomic species of marine crabs is discussed and provides evidence that crabs can be used as indicator organisms of biomarker significance for marine pollution. Overall, larval stages appeared to be the most sensitive to the deleterious effects of PH compared with juveniles and adults. However, adult stages have received more research attention than other life stages, followed by larval stages, and juvenile stages are the least investigated stages with respect to PH toxicity. Finally, hepatopancreas and gills were the organs where greatest accumulation of PH was recorded.

Keywords

Crabsdispersantlarvaemarineoilpetroleum hydrocarbonssedimentstoxicity
Type
Review
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 101 , Issue 3 , May 2021 , pp. 561 - 576
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Afifi, M, Alkaladi, A, Abu Zinada, OA and Couderchet, M (2017) Alteration in antioxidant genes expression in some fish caught from Jeddah and Yanbu coast as a bio-indicator of oil hydrocarbons pollution. Saudi Journal of Biological Sciences 24, 1580–1587.CrossRefGoogle ScholarPubMed
Akhbarizadeh, R, Moore, F and Keshavarzi, B (2019) Polycyclic aromatic hydrocarbons and potentially toxic elements in seafood from the Persian Gulf: presence, trophic transfer, and chronic intake risk assessment. Environmental Geochemistry and Health 41, 2803–2820.CrossRefGoogle ScholarPubMed
Alloy, MM, Boube, I, Griffitt, RJ, Oris, JT and Roberts, AP (2015) Photo-induced toxicity of Deepwater Horizon slick oil to blue crab (Callinectes sapidus) larvae. Environmental Toxicology and Chemistry 34, 2061–2066.10.1002/etc.3026CrossRefGoogle ScholarPubMed
Al-Wazzan, Z, Le Vay, L, Behbehani, M and Giménez, L (2020) Scale-dependent spatial and temporal patterns of abundance and population structure of the xanthid crab Leptodius exaratus on rocky shores in Kuwait. Regional Studies in Marine Science 37, 101325.10.1016/j.rsma.2020.101325CrossRefGoogle Scholar
Anderson, JA, Kuhl, AJ and Anderson, AN (2014) Toxicity of oil and dispersed oil on juvenile mud crabs, Rhithropanopeus harrisii. Bulletin of Environmental Contamination and Toxicology 92, 375–380.10.1007/s00128-014-1216-7CrossRefGoogle ScholarPubMed
Barth, H-J (2007) Crab induced salt marsh regeneration after the 1991 Gulf War oil spill. Aquatic Ecosystem Health & Management 10, 327–334.10.1080/14634980701512624CrossRefGoogle Scholar
Baumard, P, Budzinski, H, Garrigues, P, Sorbe, JC, Burgeot, T and Bellocq, J (1998) Concentrations of PAHs (polycyclic aromatic hydrocarbons) in various marine organisms in relation to those in sediments and to trophic level. Marine Pollution Bulletin 36, 951–960.10.1016/S0025-326X(98)00088-5CrossRefGoogle Scholar
Beg, MU, Butt, SA, Al-Dufaileej, S, Karam, Q, Al-Sharrah, TK and Saeed, T (2018) Biomarkers in fish as a measure of the state of marine environment of Kuwait. Environmental Monitoring and Assessment 190, 1–12.10.1007/s10661-018-6704-5CrossRefGoogle ScholarPubMed
Benson, NU, Essien, JP, Williams, AB and Ebong, GA (2007) Petroleum hydrocarbons accumulation potential of shellfishes from littoral waters of the Bight of Bonny, Niger Delta, Nigeria. Research Journal of Environmental Sciences 1, 11–19.Google Scholar
Ben-Khedher, S, Jebali, J, Kamel, N, Banni, M, Rameh, M, Jrad, A and Boussetta, H (2013) Biochemical effects in crabs (Carcinus maenas) and contamination levels in the Bizerta Lagoon: an integrated approach in biomonitoring of marine complex pollution. Environmental Science and Pollution Research 20, 2616–2631.CrossRefGoogle ScholarPubMed
Bigford, TE (1977) Effects of oil on behavioral responses to light, pressure and gravity in larvae of the rock crab Cancer irroratus. Marine Biology 43, 137–148.CrossRefGoogle Scholar
Bookhout, CG, Costlow, JD and Monroe, R (1976) Effects of methoxychlor on larval development of mud-crab and blue crab. Water, Air, and Soil Pollution 5, 349–365.10.1007/BF00158350CrossRefGoogle Scholar
Bridges, KN, Alloy, MM, Damare, L, Palmer, I, Forth, HP, Morris, J, Stoeckel, JA and Roberts, AP (2020) Planktonic fiddler crab (Uca longisignalis) are susceptible to photoinduced toxicity following in ovo exposure in oiled mesocosms. Environmental Science and Technology 54, 6254–6261.10.1021/acs.est.0c00215CrossRefGoogle ScholarPubMed
Brodersen, CC, Rice, SD, Short, JW, Mecklenburg, TA and Karinen, JF (1977) Sensitivity of larval and adult Alaskan shrimp and crabs to acute exposures of the water-soluble fraction of Cook Inlet crude oil. In International Oil Spill Conference, IOSC. pp. 575–578.10.7901/2169-3358-1977-1-575CrossRefGoogle Scholar
Brodie, RJ, Styles, R, Borgianini, S, Godley, J and Butler, K (2007) Larval mortality during export to the sea in the fiddler crab Uca minax. Marine Biology 152, 1283–1291.10.1007/s00227-007-0777-yCrossRefGoogle Scholar
Burns, KA (1976) Hydrocarbon metabolism in the intertidal fiddler crab Uca pugnax. Marine Biology 36, 5–11.CrossRefGoogle Scholar
Caldwell, RS, Caldarone, EM and Mallon, MH (1977) Effects of a seawater-soluble fraction of Cook Inlet crude oil and its major aromatic components on larval stages of the Dungeness crab, Cancer magister dana. In Wolfe DA (ed.), Fate and Effects of Petroleum Hydrocarbons in Marine Ecosystems and Organisms. New York, NY: Pergamon Press, pp. 210–220.10.1016/B978-0-08-021613-3.50027-9CrossRefGoogle Scholar
Cantelmo, AC, Lazell, RJ and Mantel, LH (1981) The effects of benzene on molting and limb regeneration in juvenile Callinectes sapidus. Marine Biology Letters 2, 333–343.Google Scholar
Cantelmo, A, Mantel, L, Lazell, R, Hospod, F, Flynn, E, Goldberg, S and Katz, M (1982) The effects of benzene and dimethyl-naphthalene on physiological processes in juveniles of the blue crab, Callinectes sapidus. In Vemberg, WB, Calabrese, A, Thurberg, FP and Vernberg, FJ (eds), Physiological Mechanisms of Marine Pollutant Toxicity. New York, NY: Academic Press, pp. 349–389.CrossRefGoogle Scholar
Carls, MG and Rice, SD (1984) Toxic contributions of specific drilling mud components to larval shrimp and crabs. Marine Environmental Research 12, 45–62.10.1016/0141-1136(84)90061-8CrossRefGoogle Scholar
Chandy, JP and Kolwalkar, DG (1984) Histological changes in the gill & hepatopancreas of the marine crabs Charybdis lucifera (Fabricius) and Scylla serrata (Forskal). Indian Journal of Marine Sciences 13, 10–13.Google Scholar
Chase, DA, Edwards, DS, Qin, G, Wages, MR, Willming, MM, Anderson, TA and Maul, JD (2013) Bioaccumulation of petroleum hydrocarbons in fiddler crabs (Uca minax) exposed to weathered MC-252 crude oil alone and in mixture with an oil dispersant. Science of the Total Environment 444, 121–127.10.1016/j.scitotenv.2012.11.078CrossRefGoogle ScholarPubMed
Chiasson, SC (2017) Spatiotemporal patterns of petroleum hydrocarbons and wastewater compounds, and their effects on growth and gene expression in the blue crab, Callinectes sapidus. PhD Thesis. Tulane University, New Orleans.Google Scholar
Chiasson, SC and Taylor, CM (2017) Effects of crude oil and oil/dispersant mixture on growth and expression of vitellogenin and heat shock protein 90 in blue crab, Callinectes sapidus, juveniles. Marine Pollution Bulletin 119, 128–132.CrossRefGoogle ScholarPubMed
Chou, CL, Paon, LA and Moffatt, JD (2002) Cadmium, copper, manganese, silver, and zinc in rock crab (Cancer irroratus) from highly copper contaminated sites in the Inner Bay of Fundy, Atlantic Canada. Bulletin of Environmental Contamination and Toxicology 68, 885–892.10.1007/s00128-002-0037-2CrossRefGoogle Scholar
Chou, CL, Paon, LA, Moffatt, JD and King, T (2003) Selection of bioindicators for monitoring marine environmental quality in the Bay of Fundy, Atlantic Canada. Marine Pollution Bulletin 46, 756–762.10.1016/S0025-326X(03)00045-6CrossRefGoogle Scholar
Chung, JY, Kim, YJ, Kim, JY, Lee, SG, Park, JE, Kim, WR, Yoon, YD, Yoo, KS, Yoo, YH and Kim, JM (2011) Benzo [α] pyrene reduces testosterone production in rat Leydig cells via a direct disturbance of testicular steroidogenic machinery. Environmental Health Perspectives 119, 1059–1074.10.1289/ehp.1003391CrossRefGoogle Scholar
Connolly, SR and Roughgarden, J (1999) Theory of Marine Communities: Competition, Predation, and Recruitment-Dependent Interaction Strength. Ecological Monographs 69. New York, NY: John Wiley & Sons.Google Scholar
Culbertson, JB, Valiela, I, Peacock, EE, Reddy, CM, Carter, A and VanderKruik, R (2007) Long-term biological effects of petroleum residues on fiddler crabs in salt marshes. Marine Pollution Bulletin 54, 955–962.10.1016/j.marpolbul.2007.02.015CrossRefGoogle ScholarPubMed
Daiber, FC (1981) Animals of the Tidal Marsh. New York, NY: Van Nostrand Reinhold.Google Scholar
Daka, ER and Ugbomeh, AP (2013) Polycyclic aromatic hydrocarbons in sediment and tissues of the crab Callinectes pallidus from the Azuabie Creek of the upper Bonny Estuary in the Niger delta. Research Journal of Applied Sciences, Engineering and Technology 6, 2594–2600.10.19026/rjaset.6.3744CrossRefGoogle Scholar
Damare, LM, Bridges, KN, Alloy, MM, Curran, TE, Soulen, BK, Forth, HP, Lay, CR, Morris, JM, Stoeckel, JA and Roberts, AP (2018) Photo-induced toxicity in early life stage fiddler crab (Uca longisignalis) following exposure to Deepwater Horizon oil. Ecotoxicology 27, 440–447.10.1007/s10646-018-1908-6CrossRefGoogle ScholarPubMed
Díaz-Jaramillo, M, Socowsky, R, Pardo, LM, Monserrat, JM and Barra, R (2013) Biochemical responses and physiological status in the crab Hemigrapsus crenulatus (Crustacea, Varunidae) from high anthropogenically-impacted estuary (Lenga, south-central Chile). Marine Environmental Research 83, 73–81.10.1016/j.marenvres.2012.10.012CrossRefGoogle Scholar
Douglas, GS, Liu, B, Wong, W, Litman, E and Hardenstine, J (2018) Red crabs as sentinel organisms in exposure of deep-Sea benthos to Macondo oil following the Deepwater Horizon oil spill. In Stout SA and Wang Z (eds), Oil Spill Environmental Forensics Case Studies. Oxford: Elsevier, pp. 651–681.10.1016/B978-0-12-804434-6.00030-6CrossRefGoogle Scholar
Epifanio, CE (1971) Effects of dieldrin in seawater on the development of two species of crab larvae, Leptodius floridanus and Panopeus herbstii. Marine Biology 11, 356–362.10.1007/BF00352454CrossRefGoogle Scholar
Fair, PA, Adams, J, Mitchum, G, Hulsey, TC, Reif, JS, Houde, M, Muir, D, Wirth, E, Wetzel, D, Zolman, E, McFee, W and Bossart, GD (2010) Contaminant blubber burdens in Atlantic bottlenose dolphins (Tursiops truncatus) from two southeastern US estuarine areas: concentrations and patterns of PCBs, pesticides, PBDEs, PFCs, and PAHs. Science of the Total Environment 408, 1577–1597.10.1016/j.scitotenv.2009.12.021CrossRefGoogle ScholarPubMed
Fern, R, Withers, K, Zimba, P, Wood, T and Schoech, L (2015) Toxicity of three dispersants alone and in combination with crude oil on blue crab Callinectes sapidus Megalopae on JSTOR. Southeastern Naturalist 14, 82–92.10.1656/058.014.0413CrossRefGoogle Scholar
Fernando, H, Ju, H, Kakumanu, R, Bhopale, KK, Croisant, S, Elferink, C, Kaphalia, BS and Ansari, GAS (2019) Distribution of petrogenic polycyclic aromatic hydrocarbons (PAHs) in seafood following Deepwater Horizon oil spill. Marine Pollution Bulletin 145, 200–207.10.1016/j.marpolbul.2019.05.015CrossRefGoogle ScholarPubMed
Fingerman, SW and Fingerman, M (1979) Comparison of the effects of fourteen-day and chronic exposures to a polychlorinated biphenyl, aroclor 1242, on molting of the fiddler crab, Uca pugilator. Bulletin of Environmental Contamination and Toxicology 21, 352–357.10.1007/BF01685435CrossRefGoogle ScholarPubMed
Firat, Ö, Gök, G, Çoǧun, HY, Yüzereroǧlu, TA and Kargin, F (2008) Concentrations of Cr, Cd, Cu, Zn and Fe in crab Charybdis longicollis and shrimp Penaeus semisulcatus from the Iskenderun Bay, Turkey. Environmental Monitoring and Assessment 147, 117–123.10.1007/s10661-007-0103-7CrossRefGoogle ScholarPubMed
Fleming, LE, Broad, K, Clement, A, Dewailly, E, Elmir, S, Knap, A, Pomponi, SA, Smith, S, Solo Gabriele, H and Walsh, P (2006) Oceans and human health: emerging public health risks in the marine environment. Marine Pollution Bulletin 53, 545–560.CrossRefGoogle ScholarPubMed
Fossi, MC, Casini, S, Savelli, C, Corbelli, C, Franchi, E, Mattei, N, Sanchez-Hernandez, JC, Corsi, I, Bamber, S and Depledge, MH (2000) Biomarker responses at different levels of biological organization in crabs (Carcinus aestuarii) experimentally exposed to benzo (α) pyrene. Chemosphere 40, 861–874.CrossRefGoogle ScholarPubMed
Franco, ME, Felgenhauer, BE and Klerks, PL (2018) Crude oil toxicity to fiddler crabs (Uca longisignalis and Uca panacea) from the northern Gulf of Mexico: impacts on bioturbation, oxidative stress, and histology of the hepatopancreas. Environmental Toxicology and Chemistry 37, 491–500.CrossRefGoogle ScholarPubMed
Frasier, KE, Solsona-Berga, A, Stokes, L and Hildebrand, JA (2020) Impacts of the Deepwater Horizon oil spill on marine mammals and sea turtles. In Murawski, SA, Ainsworth, CH, Gilbert, S, Hollander, DJ, Paris, CB, Schlüter, M and DL, Wetzel (eds), Deep Oil Spills: Facts, Fate, and Effects. Cham: Springer International Publishing, pp. 431–462.CrossRefGoogle Scholar
Fulford, R, Griffit, R, Brown-Peterson, N, Perry, H and Sanchez-Rubio, G (2014) Impacts of the Deepwater Horizon oil spill on blue crab, Callinectes sapidus, larval settlement in Mississippi. In Alford, JB, Peterson, MS and Green, CC (eds), Impacts of Oil Spill Disasters on Marine Habitats and Fisheries in North America: New York, NY: CRC Press, pp. 253–268.Google Scholar
Geiszler, PC, Grantham, BJ and Blomquist, GJ (1977) Fate of labeled n-alkanes in the blue crab and stripped mullet. Bulletin of Environmental Contamination and Toxicology 17, 463–467.CrossRefGoogle ScholarPubMed
Gelpi, CG Jr, Condrey, RE, Fleeger, JW and Dubois, SF (2009) Discovery, evaluation, and implications of blue crab, Callinectes sapidus, spawning, hatching, and foraging grounds in federal (US) waters offshore of Louisiana. Bulletin of Marine Science 8, 203–222.Google Scholar
Ghaeni, M, Pour, NA and Hosseini, M (2015) Bioaccumulation of polychlorinated biphenyl (PCB), polycyclic aromatic hydrocarbon (PAH), mercury, methyl mercury, and arsenic in blue crab Portunus segnis from Persian Gulf. Environmental Monitoring and Assessment 187, 1–9.CrossRefGoogle Scholar
Gharrett, JA and Rice, SD (1987) Influence of simulated tidal cycles on aromatic hydrocarbon uptake and elimination by the shore crab Hemigrapsus nudus. Marine Biology 95, 365–370.CrossRefGoogle Scholar
Giltz, SM and Taylor, CM (2017) Sublethal toxicity of crude oil exposure in the blue crab, Callinectes sapidus, at two life history stages. Bulletin of Environmental Contamination and Toxicology 98, 178–182.CrossRefGoogle ScholarPubMed
Giménez, L (2002) Effects of prehatching salinity and initial larval biomass on survival and duration of development in the zoea 1 of the estuarine crab, Chasmagnathus granulata, under nutritional stress. Journal of Experimental Marine Biology and Ecology 270, 93–110.CrossRefGoogle Scholar
Gospodarek, J, Petryszak, P, Kołoczek, H and Rusin, M (2019) The effect of soil pollution with petroleum-derived substances on Porcellio scaber Latr. (Crustacea, Isopoda). Environmental Monitoring and Assessment 191, 1–10.CrossRefGoogle Scholar
Guls, HD (2020) Accumulation and Biomarker Responses in the Atlantic Rock Crab (Cancer irroratus) Exposed to Benzo(a)Pyrene Through Ingestion of Contaminated Mussels (Mytilus edulis). University of Iceland: Reykjavik.Google Scholar
Habibullah-Al-Mamun Md, Ahmed MK, Saiful, MI, Tokumura, M and Masahiro, S (2019) Distribution of polycyclic aromatic hydrocarbons (PAHs) in commonly consumed seafood from coastal areas of Bangladesh and associated human health implications. Environmental Geochemistry and Health 41, 1105–1121.CrossRefGoogle Scholar
Hale, RC (1988) Disposition of polycyclic aromatic compounds in blue crabs, Callinectes sapidus, from the southern Chesapeake Bay. Estuaries 11, 255–263.CrossRefGoogle Scholar
Hartman, MJ and Sulkin, S (1999) Effects of prior exposure to petroleum hydrocarbon contamination during brooding on the subsequent larval development of the brachyuran crab Hemigrapsus oregonensis. Journal of Crustacean Biology 19, 690–698.CrossRefGoogle Scholar
Hyland, JL and Schneider, ED (1976) Petroleum hydrocarbons and their effects on marine organisms, populations, communities, and ecosystems. In Effects and Sinks of Hydrocarbons in the Aquatic Environment. Washington, DC: American Institute of Biological Sciences, pp. 463–506.Google Scholar
Jebali, J, Chicano-Gálvez, E, Fernández-Cisnal, R, Banni, M, Chouba, L, Boussetta, H, López-Barea, J and Alhama, J (2014) Proteomic analysis in caged Mediterranean crab (Carcinus maenas) and chemical contaminant exposure in Téboulba Harbour, Tunisia. Ecotoxicology and Environmental Safety 100, 15–26.CrossRefGoogle ScholarPubMed
Karam, Q, Ali, M, Subrahmanyam, M, Al-Abdul, K, Bentley, M, Beg, M, Pandey Penelope Watt, AJ and Al-Abdul Elah, K (2019) A comparative study on the effect of dispersed and undispersed Kuwait crude oil on egg hatching and larval survival of Epinephelus coioides. Journal of Environmental Biology 192, 192–199.CrossRefGoogle Scholar
Karam, Q, Beg, MU, Al-Khabbaz, A, Al-Ballam, Z, Dakour, S and Al-Abdul Elah, K (2014) Effect of water accommodated fraction of Kuwait crude oil on developmental stages of orange-spotted grouper hamoor (Epinephelus coicoides). International Journal of Advances in Agricultural and Environmental Engineering 1, 105–112.Google Scholar
Katz, LM (1973) The effects of water soluble fraction of crude oil on larvae of the decapod crustacean Neopanope texana (Sayi). Environmental Pollution 5, 199–204.Google Scholar
Kennish, R, Williams, GA and Lee, SY (1996) Algal seasonality on an exposed rocky shore in Hong Kong and the dietary implications for the herbivorous Grapsus albolineatus. Marine Biology 125, 55–64.CrossRefGoogle Scholar
Kittredge, JS, Takahashi, FT, Lindsey, J and Lasker, R (1974) Chemical signals in the sea: marine allelochemics and evolution. Fishery Bulletin 72, l–ll.Google Scholar
Knap, A, Turner, NR, Bera, G, Renegar, DA, Frank, T, Sericano, J and Riegl, BM (2017) Short-term toxicity of 1-methylnaphthalene to Americamysis bahia and 5 deep-sea crustaceans. Environmental Toxicology and Chemistry 36, 3415–3423.CrossRefGoogle ScholarPubMed
Krebs, CT and Burns, KA (1977) Long-term effects of an oil spill on populations of the salt-marsh crab Uca pugnax. Science (New York, N.Y.) 197, 484–487.CrossRefGoogle ScholarPubMed
Krebs, CT and Burns, KA (1978) Long-term effects of an oil spill on populations of the salt-marsh crab Uca pugnax. Journal of the Fisheries Research Board of Canada 35, 648–649.CrossRefGoogle Scholar
Kujawinski, EB, Soule, MCK, Valentine, DL, Boysen, AK, Longnecker, K and Redmond, MC (2011) Fate of dispersants associated with the Deepwater Horizon oil spill. Environmental Science and Technology 45, 1298–1306.CrossRefGoogle ScholarPubMed
Kulkarni, BG and Masurekar, VB (1984) Effects of naphthalene exposure on blood serum enzyme activities in the crab Scylla serrata (Forskal). Indian Journal of Marine Sciences 13, 97–98.Google Scholar
Lai, JCY, Ng, PKL and Davie, PJF (2010) A revision of the Portunus pelagicus (Linnaeus, 1758) species complex (Crustacea: Brachyura: Portunidae), with the recognition of four species. Raffles Bulletin of Zoology 58, 199–237.Google Scholar
Lance, BK, Irons, DB, Kendall, SJ and McDonald, LL (2001) An evaluation of marine bird population trends following the Exxon Valdez oil spill, Prince William Sound, Alaska. Marine Pollution Bulletin 42, 298–309.CrossRefGoogle Scholar
Laughlin, RB and Neff, JM (1980) Influence of temperature, salinity, and phenanthrene (a petroleum derived polycyclic aromatic hydrocarbon) on the respiration of larval mud crabs, Rhithropanopeus harrisii. Estuarine and Coastal Marine Science 10, 655–669.CrossRefGoogle Scholar
Laughlin, RB and Neff, JM (1981) Ontogeny of respiratory and growth responses of larval mud crabs Rhithropanopeus harrisii exposed to different temperatures, salinities and naphthalene concentrations. Marine Ecology Progress Series 5, 319–332.CrossRefGoogle Scholar
Laughlin, RB, Young, LGL and Neff, JM (1978) A long-term study of the effects of water-soluble fractions of No. 2 fuel oil on the survival, development rate, and growth of the mud crab Rhithropanopeus harrisii. Marine Biology 47, 87–95.CrossRefGoogle Scholar
Laurén, DJ and Rice, S (1985) Significance of active and passive depuration in the clearance of naphthalene from the tissues of Hemigrapsus nudus (Crustacea: Decapoda). Marine Biology 88, 135–142.CrossRefGoogle Scholar
Lee, RF, Ryan, C and Neuhauser, ML (1976) Fate of petroleum hydrocarbons taken up from food and water by the blue crab Callinectes sapidus. Marine Biology 37, 363–370.CrossRefGoogle Scholar
Lin, T, Hu, L, Guo, Z, Zhang, G and Yang, Z (2013) Deposition fluxes and fate of polycyclic aromatic hydrocarbons in the Yangtze River estuarine-inner shelf in the East China Sea. Global Biogeochemical Cycles 27, 77–87.CrossRefGoogle Scholar
Lively, JAA and Mckenzie, J (2014) Toxicity of the dispersant corexit 9500 to early life stages of blue crab, Callinectes sapidus. Bulletin of Environmental Contamination and Toxicology 93, 649–653.CrossRefGoogle Scholar
Mahugija, JAM, Ahmed, KN and Makame, YMM (2017) Polycyclic aromatic hydrocarbons (PAHs) contamination in coastal mangrove ecosystems of the Zanzibar archipelago. Western Indian Ocean Journal of Marine Science 16, 25–34.Google Scholar
Malan, DE (1988) The effects of Qatar light crude oil on the saltmarsh crab Sesarma caienata and its implications in the field: toxicity to adults and larvae. South African Journal of Marine Science 7, 37–44.CrossRefGoogle Scholar
Marshall, DJ, Bonduriansky, R and Bussière, LF (2008) Offspring size variation within broods as a bet-hedging strategy in unpredictable environments. Ecology 89, 2506–2517.CrossRefGoogle ScholarPubMed
McElroy, AE, Farrington, JW and Teal, JM (1989) Bioavailability of polycyclic aromatic hydrocarbons in the aquatic environment. In Varanasi, U (ed.), Metabolism of Polycyclic Aromatic Hydrocarbons in the Aquatic Environment. Boca Raton, FL: CRC Press, pp. 1–39.Google Scholar
Meador, JP, Stein, JE, Reichert, WL and Varanasi, U (1995) Bioaccumulation of polycyclic aromatic hydrocarbons by marine organisms. Reviews of Environmental Contamination and Toxicology. New York, NY: Springer.Google Scholar
Mecklenburg, TA, Rice, SD and Karinen, JF (1977) Molting and survival of king crab (Paralithodes camtschatica) and coonstripe shrimp (Pandalus hypsinotus) larvae exposed to Cook Inlet crude oil water-soluble fraction. In Wolfe DA (ed.), Fate and Effects of Petroleum Hydrocarbons in Marine Ecosystems and Organisms. New York, NY: Pergamon Press, pp. 221–228.CrossRefGoogle Scholar
Melzian, BD and Lake, J (1986) Accumulation and retention of no. 2 fuel oil compounds in the blue crab, Callinectes sapidus Rathbun. Oil and Chemical Pollution 3, 367–399.CrossRefGoogle Scholar
Mironov, OG (1980) Aspects of petroleum hydrocarbon metabolism in marine animals. Helgoländer Meeresuntersuchungen 33, 292–296.CrossRefGoogle Scholar
Monikh, FA, Hosseini, M and Rahmanpour, S (2014) The effect of size and sex on PCB and PAH concentrations in crab Portunus pelagicus. Environmental Monitoring and Assessment 186, 1575–1582.CrossRefGoogle Scholar
Montague, CL (1980) A natural history of temperate western Atlantic fiddler crab (genus Uca) with reference to their impact on the salt marsh. Contributions in Marine Science 23, 25–55.Google Scholar
Moon, HB, An, YR, Park, KJ, Choi, SG, Moon, DY, Choi, M and Choi, HG (2011) Occurrence and accumulation features of polycyclic aromatic hydrocarbons and synthetic musk compounds in finless porpoises (Neophocaena phocaenoides) from Korean coastal waters. Marine Pollution Bulletin 62, 1963–1968.CrossRefGoogle ScholarPubMed
Morgan, SG (1987) Adaptive significance of hatching rhythms and dispersal patterns of estuarine crab larvae: avoidance of physiological stress by larval export? Journal of Experimental Marine Biology and Ecology 113, 71–78.CrossRefGoogle Scholar
Mothershead, RF and Hale, RC (1992) Influence of ecdysis on the accumulation of polycyclic aromatic hydrocarbons in field exposed blue crabs (Callinectes sapidus). Marine Environmental Research 33, 145–156.CrossRefGoogle Scholar
Mothershead, RF, Hale, RC and Greaves, J (1991) Xenobiotic compounds in blue crabs from a highly contaminated urban subestuary. Environmental Toxicology and Chemistry 10, 1341–1349.CrossRefGoogle Scholar
Mouton, EC and Felder, DL (1995) Reproduction of the fiddler crabs Uca longisignalis and Uca spinicarpa in a Gulf of Mexico salt marsh. Estuaries 18, 469–481.CrossRefGoogle Scholar
Muggelberg, LL (2013) Trophic Response To Polycyclic Aromatic Hydrocarbons and Copper Exposure in Tidal Flats of North Inlet, South Carolina. University of South Carolina, South Carolina, https://scholarcommons.sc.edu/etd/2360.Google Scholar
Nakata, H, Sakai, Y, Miyawaki, T and Takemura, A (2003) Bioaccumulation and toxic potencies of polychlorinated biphenyls and polycyclic aromatic hydrocarbons in tidal flat and coastal ecosystems of the Ariake Sea, Japan. Environmental Science and Technology 37, 3513–3521.CrossRefGoogle ScholarPubMed
Ng, PKL, Lin, CW and Ho, PH (2018) On three species of reef-dwelling pilumnid crabs from Taiwan, with notes on Heteropilumnus De Man, 1895 (Crustacea: Brachyura). Zoological Studies 57, 12.Google Scholar
Nkpaa, KW, Essien, EB and Wegwu, MO (2013) Evaluation of polycyclic aromatic hydrocarbon (PAH) concentrations in crabs and shrimps from crude oil polluted waters of Ogoniland in Rivers State, Nigeria. IOSR Journal Of Environmental Science, Toxicology and Food Technology 4, 73–80.CrossRefGoogle Scholar
Nozar, SLM, Pauzi, MZ, Salarpouri, A, Daghooghi, B and Salimizadeh, M (2015) Total petroleum hydrocarbons in edible marine biota from Northern Persian Gulf. Environmental Monitoring and Assessment 187, 1–6.CrossRefGoogle ScholarPubMed
Olayinka, OO, Adewusi, AA, Olujimi, OO and Aladesida, AA (2019) Polycyclic aromatic hydrocarbons in sediment and health risk of fish, crab and shrimp around Atlas Cove, Nigeria. Journal of Health & Pollution 9, 1–21.CrossRefGoogle ScholarPubMed
Ololade, I, Lajide, L and Amoo, I (2008) Occurrence and toxicity of hydrocarbon residues in crab (Callinectes sapidus) from contaminated site. Journal of Applied Sciences and Environmental Management 12, 19–23.Google Scholar
Ong, MC, Tan, YF, Khoo, XY and Yong, JC (2015) Heavy metals and polycyclic aromatic hydrocarbons (PAHs) concentration in mud crab (Scylla serrata) from UMT Mangrove, Terengganu, Malaysia. Advances in Environmental Biology 9, 66–74.Google Scholar
Ozhan, K, Parsons, ML and Bargu, S (2014) How were phytoplankton affected by the deepwater horizon oil spill? BioScience 64, 829–836.CrossRefGoogle Scholar
Paital, B and Chainy, GBN (2010) Antioxidant defenses and oxidative stress parameters in tissues of mud crab (Scylla serrata) with reference to changing salinity. Comparative Biochemistry and Physiology – C Toxicology and Pharmacology 151, 142–151.CrossRefGoogle ScholarPubMed
Pearson, WH and Olla, BL (1979) Detection of naphthalene by the blue crab, Callinectes sapidus. Estuaries 2, 64–65.CrossRefGoogle Scholar
Pearson, WH and Olla, BL (1980) Threshold for detection of naphthalene and other behavioral responses by the blue crab, Callinectes sapidus. Estuaries 3, 224–229.CrossRefGoogle Scholar
Pearson, WH, Miller, SE, Blaylock, JW and Olla, BL (1981) Detection of the water-soluble fraction of crude oil by the blue crab, Callinectes sapidus. Marine Environmental Research 5, 3–11.CrossRefGoogle Scholar
Pearson, WH, Skalski, JR, Sulkin, SD and Malme, CI (1994) Effects of seismic energy releases on the survival and development of zoeal larvae of Dungeness crab (Cancer magister). Marine Environmental Research 38, 93–113.CrossRefGoogle Scholar
Pechenik, JA (2006) Larval experience and latent effects – metamorphosis is not a new beginning. Integrative and Comparative Biology 46, 323–333.CrossRefGoogle Scholar
Phukaokaew, S, Sukhsangchan, C and Meksumpun, S (2015) Petroleum hydrocarbon's quantity and impact on soldier crab after crude oil spilled hits Ao Phrao beach, Koh Samet, Rayong Province. In The 53rd Kasetsart University Annual Conference. Bangkok: Kasetsart University, pp. 1263–1270.Google Scholar
Pie, HV, Schott, EJ and Mitchelmore, CL (2015) Investigating physiological, cellular and molecular effects in juvenile blue crab, Callinectus sapidus, exposed to field-collected sediments contaminated by oil from the Deepwater Horizon incident. Science of the Total Environment 532, 528–539.CrossRefGoogle ScholarPubMed
Robinson, AG and Dillaman, RM (1985) The effects of naphthalene on the ultrastructure of the hepatopancreas of the fiddler crab, Uca minax. Journal of Invertebrate Pathology 45, 311–323.CrossRefGoogle Scholar
Robinson, EM and Rabalais, NN (2019) The effects of oil on blue crab and periwinkle snail interactions: a mesocosm study. Journal of Experimental Marine Biology and Ecology 517, 34–39.CrossRefGoogle Scholar
Romero, AF, Oliveira, M and Abessa, DMS (2018) A simple bird sensitivity to oil index as a management tool in coastal and marine areas subject to oil spills when few biological information is available. Marine Pollution Bulletin 128, 460–465.CrossRefGoogle ScholarPubMed
Sabourin, TD (1982) Respiratory and circulatory responses of the blue crab to naphthalene and the effect of acclimation salinity. Aquatic Toxicology 2, 301–318.CrossRefGoogle Scholar
Saeed, T and Al-Mutairi, M (1999) Chemical composition of the watersoluble fraction of the leaded gasolines in seawater. Environment International 25, 117–129.CrossRefGoogle Scholar
Samiullah, Y (1985) Biological effects of marine oil pollution. Oil and Petrochemical Pollution 2, 235–264.CrossRefGoogle Scholar
Sammarco, PW, Kolian, SR, Warby, RAF, Bouldin, JL, Subra, WA and Porter, SA (2013) Distribution and concentrations of petroleum hydrocarbons associated with the BP/Deepwater Horizon Oil Spill, Gulf of Mexico. Marine Pollution Bulletin 73, 129–143.CrossRefGoogle Scholar
Schimmel, SC, Patrick, JM, Faas, LF, Oglesby, JL and Wilson, AJ (1979) Kepone: toxicity and bioaccumulation in blue crabs. Estuaries 2, 9–15.CrossRefGoogle Scholar
Schmitt, B and Ache, BW (1979) Olfaction: responses of a decapod crustacean are enhanced by flicking. Science 205, 204–206.CrossRefGoogle ScholarPubMed
Shih, HT, Ng, PKL, Davie, PJF, Schubart, CD, Türkay, M, Naderloo, R, Jones, D and Liu, MY (2016) Systematics of the family Ocypodidae Rafinesque, 1815 (Crustacea: Brachyura), based on phylogenetic relationships, with a reorganization of subfamily rankings and a review of the taxonomic status of Uca Leach, 1814, sensu lato and its subgenera. Raffles Bulletin of Zoology 64, 139–175.Google Scholar
Soares-Gomes, A, Neves, RL, Aucélio, R, Van Der Ven, PH, Pitombo, FB, Mendes, CLT, and Ziolli, RL (2010) Changes and variations of polycyclic aromatic hydrocarbon concentrations in fish, barnacles and crabs following an oil spill in a mangrove of Guanabara Bay, Southeast Brazil. Marine Pollution Bulletin 60, 1359–1363.CrossRefGoogle Scholar
Singer, SC and Lee, RF (1977) Mixed function oxygenase activity in blue crab, Callinectes sapidus: tissue distribution and correlation with changes during molting and development. Biological Bulletin 153, 377–386.CrossRefGoogle Scholar
Sinski, J, Perry, HM and Exner, J (2016) Assessing petroleum contamination in blue crab Callinectes sapidus megalopae using fluorescence spectroscopy. Journal of Shellfish Research 35, 1–12.CrossRefGoogle Scholar
Spicer, JI and Weber, RE (1991) Respiratory impairment in crustaceans and molluscs due to exposure to heavy metals. Comparative Biochemistry and Physiology. C, Comparative Pharmacology and Toxicology 100, 339–342.CrossRefGoogle ScholarPubMed
Spivak, E, Anger, K, Luppi, T, Bas, C and Ismael, D (1994) Distribution and habitat preferences of 2 grapsid crab species in Mar-Chiquita Lagoon (Province of Buenos-Aires, Argentina). Helgolander Meeresuntersuchungen 48, 59–78.CrossRefGoogle Scholar
Sprague, JB (1970) Measurement of pollutant toxicity to fish. II. Utilizing and applying bioassay results. Water Research 4, 3–32.CrossRefGoogle Scholar
Stickle, WB (2002) Effects of Simultaneous Exposure to Petroleum Hydrocarbons, Hypoxia, and Prior Exposure on the Tolerance and Sublethal Responses of Marine Animals: Blue Crabs and Killifish Final Report. U.S. Dept. of the Interior, Minerals Management Service, Gulf of Mexico OCS Region, New Orleans, LA.Google Scholar
Sun, RX, Lin, Q, Ke, CL, Du, FY, Gu, YG, Cao, K, Luo, XJ and Mai, BX (2016) Polycyclic aromatic hydrocarbons in surface sediments and marine organisms from the Daya Bay, South China. Marine Pollution Bulletin 103, 325–332.CrossRefGoogle ScholarPubMed
Sun, R, Sun, Y, Li, QX, Zheng, X, Luo, X and Mai, B (2018) Polycyclic aromatic hydrocarbons in sediments and marine organisms: implications of anthropogenic effects on the coastal environment. Science of the Total Environment 640–641, 264–272.CrossRefGoogle ScholarPubMed
Takahashi, FT and Kittredge, JS (1973) Sublethal effects of the water soluble component of oil: chemical communication in the marine environment. In Ahearn, DG and Meyers, SP (eds), The Microbial Degradation of Oil Pollutants. Baton Rouge, LA: Louisiana State University Press, Pub. LSU-SG-73-01, pp. 259–264.Google Scholar
Taylor, LM (2015) Photox Induced Toxicity in Early Lifestage Fiddler Crab (Uca longisignalis) Following Exposure to Deepwater Horizon spill oil. TX: University of North Texas, TX.Google Scholar
Teal, JM (1962) Energy flow in the salt marsh ecosystem of Georgia. Ecology 43, 614–624.CrossRefGoogle Scholar
Teal, JM, Farrington, JW, Burns, KA, Stegeman, JJ, Tripp, BW, Woodin, B and Phinney, C (1992) The West Falmouth oil spill after 20 years: fate of fuel oil compounds and effects on animals. Marine Pollution Bulletin 24, 607–614.CrossRefGoogle Scholar
Theuerkauff, D, Rivera-Ingraham, GA, Roques, JAC, Azzopardi, L, Bertini, M, Lejeune, M, Farcy, E, Lignot, J and Sucré, E (2018) Salinity variation in a mangrove ecosystem: a physiological investigation to assess potential consequences of salinity disturbances on mangrove crabs. Zoological Studies 57, 36.Google Scholar
Tian, S, Pan, L and Zhang, H (2014) Identification of a CYP3A-like gene and CYPs mRNA expression modulation following exposure to benzo[a] pyrene in the bivalve mollusk Chlamys farreri. Marine Environmental Research 94, 7–15.CrossRefGoogle Scholar
Uthe, JF and Musial, CJ (1986) Polycyclic aromatic hydrocarbon contamination of American lobster, Homarus americanus, in the proximity of a coal-coking plant. Bulletin of Environmental Contamination and Toxicology 37, 730–738.CrossRefGoogle ScholarPubMed
Vandermeulen, JH, Hanrahan, J and Hemsworth, T (1980) Respiratory changes and stability of haemocyanin–O2 binding capacity in the crab cancer irroratus exposed to Kuwait crude oil in sea water. Marine Environmental Research 3, 161–170.CrossRefGoogle Scholar
Varanasi, U and Malin, D (1977) Metabolism of petroleum hydrocarbons: accumulation and biotransformation in marine organisms. In Malins, DC (ed.), Effects of Petroleum on Arctic and Subarctic Marine Environments and Organisms. New York, NY: Academic Press, pp. 176–269.Google Scholar
Vijayavel, K, Anbuselvam, C, Balasubramanian, MP, Deepak Samuel, V and Gopalakrishnan, S (2006) Assessment of biochemical components and enzyme activities in the estuarine crab Scylla tranquebarica from naphthalene contaminated habitants. Ecotoxicology 15, 469–476.CrossRefGoogle ScholarPubMed
Vijayavel, K and Balasubramanian, MP (2006) Changes in oxygen consumption and respiratory enzymes as stress indicators in an estuarine edible crab Scylla serrata exposed to naphthalene. Chemosphere 63, 1523–1531.CrossRefGoogle Scholar
Vijayavel, K, Gomathi, RD, Durgabhavani, K and Balasubramanian, MP (2004) Sublethal effect of naphthalene on lipid peroxidation and antioxidant status in the edible marine crab Scylla serrata. Marine Pollution Bulletin 48, 429–433.CrossRefGoogle ScholarPubMed
Walker, TR, MacAskill, D and Weaver, P (2013) Legacy contaminant bioaccumulation in rock crabs in Sydney Harbour during remediation of the Sydney Tar Ponds, Nova Scotia, Canada. Marine Pollution Bulletin 77, 412–417.CrossRefGoogle ScholarPubMed
Walsh, PJ and Henry, RP (1990) Activities of metabolic enzymes in the deep-water crabs Chaceon fenneri and C. quinquedens and the shallow-water crab Callinectes sapidus. Marine Biology 106, 343–346.CrossRefGoogle Scholar
Wang, SY and Stickle, WB (1987) Bioenergetics, growth and molting of the blue crab, Callinectes sapidus, exposed to the water-soluble fraction of south Louisiana crude oil. In Vernberg, WB, Winona, B, Calabrese, A, Thurberg, FP and Vernberg, FJ (eds), Pollution Physiology of Estuarine Organisms. Columbia, SC: University of South Carolina Press, pp. 107–126.Google Scholar
Wang, SY and Stickle, WB (1988) Biochemical composition of the blue crab Callinectes sapidus exposed to the water-soluble fraction of crude oil. Marine Biology 98, 23–30.CrossRefGoogle Scholar
Wang, JQ, Zhang, XD, Jiang, LF, Bertness, MD, Fang, CM, Chen, JK, Hara, T and Li, B (2010) Bioturbation of burrowing crabs promotes sediment turnover and carbon and nitrogen movements in an estuarine salt marsh. Ecosystems 13, 586–599.CrossRefGoogle Scholar
Weis, JS (2012) Walking Sideways: The Remarkable World of Crabs. Ithaca, NY: Cornell University Press.CrossRefGoogle Scholar
Weiss, M, Heilmayer, O, Brey, T and Thatje, S (2009) Influence of temperature on the zoeal development and elemental composition of the cancrid crab, Cancer setosus Molina, 1782 from Pacific South America. Journal of Experimental Marine Biology and Ecology 376, 48–54.CrossRefGoogle Scholar
Wen, J and Pan, L (2016) Short-term exposure to benzo[a]pyrene causes oxidative damage and affects haemolymph steroid levels in female crab Portunus trituberculatus. Environmental Pollution 208, 486–494.CrossRefGoogle Scholar
Wolfe, MF, Schwartz, GJB, Singaram, S, Mielbrecht, EE, Tjeerdema, RS and Sowby, ML (1996) Influence of dispersants on trophic transfer of petroleum hydrocarbons in a marine food chain. Spill Science and Technology Bulletin 3, 255–258.CrossRefGoogle Scholar
Wolfe, MF, Schwartz, GJB, Singaram, S, Mielbrecht, EE, Tjeerdema, RS and Sowby, ML (2001) Influence of dispersants on the bioavailability and trophic transfer of petroleum hydrocarbons to larval topsmelt (Atherinops affinis). Aquatic Toxicology 52, 49–60.CrossRefGoogle Scholar
Wu, X, Cheng, Y, Zeng, C, Wang, C and Yang, X (2010) Reproductive performance and offspring quality of wild-caught and pond-reared swimming crab Portunus trituberculatus broodstock. Aquaculture 301, 78–84.CrossRefGoogle Scholar
Wu, XG, Yao, GG, Yang, XZ, Cheng, YX and Wang, CL (2007) A study on the ovarian development of Portunus trituberculatus in East China Sea during the first reproductive cycle. Acta Oceanologica Sinica 29, 120–127.Google Scholar
Xia, K, Hagood, G, Childers, C, Atkins, J, Rogers, B, Ware, L, Armbrust, K, Jewell, J, Diaz, D, Gatian, N and Folmer, H (2012) Polycyclic aromatic hydrocarbons (PAHs) in Mississippi seafood from areas affected by the Deepwater Horizon oil spill. Environmental Science and Technology 46, 5310–5318.CrossRefGoogle ScholarPubMed
Yednock, BK, Sullivan, TJ and Neigel, JE (2015) De novo assembly of a transcriptome from juvenile blue crabs (Callinectes sapidus) following exposure to surrogate Macondo crude oil. BMC Genomics 16, 1–15.CrossRefGoogle ScholarPubMed
Ylitalo, G, Collier, T, Anulacion, B, Juaire, K, Boyer, R, da Silva, D, Keene, J and Stacy, B (2017) Determining oil and dispersant exposure in sea turtles from the northern Gulf of Mexico resulting from the Deepwater Horizon oil spill. Endangered Species Research 33, 9–24.CrossRefGoogle Scholar
Yu, N, Ding, Q, Li, E, Qin, JG, Chen, L and Wang, X (2018) Growth, energy metabolism and transcriptomic responses in Chinese mitten crab (Eriocheir sinensis) to benzo[Α]pyrene (BaP) toxicity. Aquatic Toxicology 203, 150–158.CrossRefGoogle Scholar
Yunker, MB, Cretney, WJ and Ikonomou, MG (2002) Assessment of chlorinated dibenzo-p-dioxin and dibenzofuran trends in sediment and crab hepatopancreas from pulp mill and harbor sites using multivariate-and index-based approaches. Environmental Science and Technology 36(9), 1869–1878.CrossRefGoogle ScholarPubMed
Zengel, S, Pennings, SC, Silliman, B, Montague, C, Weaver, J, Deis, DR, Krasnec, MO, Rutherford, N and Nixon, Z (2016) Deepwater Horizon oil spill impacts on salt marsh fiddler crabs (Uca spp.). Estuaries and Coasts 39, 1154–1163.CrossRefGoogle Scholar
Zhang, C, Li, Y, Wang, C, Feng, Z, Hao, Z, Yu, W, Wang, T and Zou, X (2020) Polycyclic aromatic hydrocarbons (PAHs) in marine organisms from two fishing grounds, South Yellow Sea, China: bioaccumulation and human health risk assessment. Marine Pollution Bulletin 153, 110995.CrossRefGoogle ScholarPubMed
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