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Advances in the aquatic sciences
RESEARCH ARTICLE

UV radiation effects on the embryos of anchoveta (Engraulis ringens) and common sardine (Strangomera bentincki) off central Chile

P. Vásquez A , A. Llanos-Rivera B E , L. R. Castro A and C. Fernandez C D
+ Author Affiliations
- Author Affiliations

A Laboratorio de Oceanografía Pesquera y Ecología Larval (LOPEL), Departamento de Oceanografía and COPAS Sur Austral Program, PO Box 160-C Concepción, Universidad de Concepción, Concepción, Chile.

B Unidad de Biotecnología Marina, Facultad de Ciencias Naturales y Oceanográficas, PO Box 160-C Concepción, Universidad de Concepción, Concepción, Chile.

C Sorbonne Universités, UPMC Univ Paris 06, CNRS, Laboratoire d’Océanographie Microbienne (LOMIC), Observatoire Océanologique, F-66650, Banyuls-sur-Mer, France.

D Interdisciplinary Center for Aquaculture Research (INCAR) and COPAS SAustral Program, PO Box 160-C Concepción, Universidad de Concepción, Concepción, Chile.

E Corresponding author. Email: alllanos@udec.cl

Marine and Freshwater Research 67(2) 195-209 https://doi.org/10.1071/MF14038
Submitted: 8 February 2014  Accepted: 22 December 2014   Published: 22 May 2015

Abstract

It has been proposed that current levels of ultraviolet B (UVB) radiation could cause lethal or sublethal effects on fish embryos located in the upper layers of the water column. Observed levels of UVB off central Chile (36°S, 73°W) indicate that planktonic fish embryos could be exposed to harmful UVB radiation. From July 2011 to January 2012 embryos from anchoveta (Engraulis ringens) and common sardine (Strangomera bentincki) were used to test experimentally whether the UVB levels in central Chile produce lethal or sublethal effects in epipelagic fish embryos. Simultaneously, whether the embryos might be exposed to harmful UVB levels in the field was investigated. Our experimental results show that UVB may cause a decrease in hatching success, changes in buoyancy and embryonic malformations. These results, along with the observed vertical distribution of embryos and UVB radiation levels in the field during late spring suggest that lethal and sublethal effects may be occurring in the embryos of both species.

Additional keywords  : embryo buoyancy, fish embryos, hatching, malformations, natural mortality, small pelagic fish, survival, vertical distribution.


References

Applegate, L., and Ley, R. (1988). Ultraviolet radiation-induced lethality and repair of pyrimidine dimers in fish embryos. Mutation Research 198, 85–92.
Ultraviolet radiation-induced lethality and repair of pyrimidine dimers in fish embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhs1Cis70%3D&md5=f838a64f94f4ec9641e87364dcc283cdCAS | 3352631PubMed |

Artüz, M. (1999). The egg and larval growth stages of Black Sea anchovy, Engraulis encrasicholus ponticus (Majorowa, 1934). Technical Paper 11/1, Fisheries Advisory Commission. Available at http://www.artuz.com/artuz/leventdeniz/levent/PDF/The%20egg%20and%20larval%20growth%20stages%20of%20Black%20Sea%20Anchovy,%20Engraulis%20encrasicholus%20ponticus%20(Majorowa,%201934).pdf [Verified 8 April 2015].

Browman, H. (2003). Assessing the impacts of solar ultraviolet radiation on the early life stages of crustacean zooplankton and ichthyoplankton in marine coastal systems. Estuaries 26, 30–39.
Assessing the impacts of solar ultraviolet radiation on the early life stages of crustacean zooplankton and ichthyoplankton in marine coastal systems.Crossref | GoogleScholarGoogle Scholar |

Cameron, P., Berg, J., Dethlefsen, V., and Von Westernhagen, H. (1992). Developmental defects in pelagic embryos of several flatfish species in the southern Netherlands. Journal of Sea Research 29, 239–256.
Developmental defects in pelagic embryos of several flatfish species in the southern Netherlands.Crossref | GoogleScholarGoogle Scholar |

Castro, L. R., Llanos, A., Blanco, J., Tarifeño, E., Escribano, R., and Landaeta, M. (2002). Influence of latitude variations in spawning habitat characteristics on the early life history traits of the anchoveta, Engraulis ringens, off northern and central Chile. GLOBEC Report 16, pp. 42-45, Global Ocean Ecosystem Dynamics. Available at http://www.globec.org/index.php?id=185 [Verified 8 April 2015].

Chilean Meteorological Office (2009). Boletín de Radiación Ultravioleta. Dirección General de Aeronáutica Civil, Subdepartamento de Climatología y Meteorología Aplicada.

Chioccara, F., Della Gala, A., De Rosa, M., Novellino, E., and Prota, G. (1980). Mycosporine aminoacids and related compounds from the eggs of fishes. Bulletin des Sociétés Chimiques Belges 89, 1101–1106.
Mycosporine aminoacids and related compounds from the eggs of fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhtlKnsLc%3D&md5=e64613a30bb96de7e33364730a6f42ecCAS |

Coombs, S. (1981). A density-gradient column for determining the specific gravity of fish eggs, with particular reference to eggs of the mackerel Scomber scombrus. Marine Biology 63, 101–106.
A density-gradient column for determining the specific gravity of fish eggs, with particular reference to eggs of the mackerel Scomber scombrus.Crossref | GoogleScholarGoogle Scholar |

Coombs, S., Boyra, G., Rueda, L., Uriarte, A., Santos, M., Conway, D., and Halliday, N. (2004). Buoyancy measurements and vertical distribution of eggs of sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus). Marine Biology 145, 959–970.
Buoyancy measurements and vertical distribution of eggs of sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus).Crossref | GoogleScholarGoogle Scholar |

Craik, J., and Harvey, S. (1987). The causes of buoyancy in eggs of marine teleosts. Journal of the Marine Biological Association of the United Kingdom 67, 169–182.
The causes of buoyancy in eggs of marine teleosts.Crossref | GoogleScholarGoogle Scholar |

Cubillos, L., Canales, T., Bucarey, D., Rojas, A., and Alarcón, R. (1999). Época reproductiva y talla media de primera madurez de Strangomera bentincki, y Engraulis ringens en el período 1993–1997 en la zona centro sur de Chile. Investigaciones Marinas 27, 73–85.
Época reproductiva y talla media de primera madurez de Strangomera bentincki, y Engraulis ringens en el período 1993–1997 en la zona centro sur de Chile.Crossref | GoogleScholarGoogle Scholar |

De Gaspar, I., Blanquez, M. J., Fraile, B., Paniagua, R., and Arenas, M. I. (1999). The hatching gland cells of trout embryos: characterisation of N- and O-linked oligosaccharides. Journal of Anatomy 194, 109–118.
The hatching gland cells of trout embryos: characterisation of N- and O-linked oligosaccharides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXislKltbY%3D&md5=faececf259bd94e86ec479535323b8b6CAS | 10227672PubMed |

Dethlefsen, V., Tüg, H., Baumann, M., Von Westernhagen, H., and Herbert, A. (1996a). Experimente über die Wirkung von UV-B auf pelagische Fischembryonen in einem Sonnenscheinsimulator. Informationen aus der Fischereiforschung 43, 180–186.

Dethlefsen, V., Von Westernhagen, H., and Cameron, P. (1996b). Malformations in North Sea pelagic fish embryos during the period 1984–1995. ICES Journal of Marine Science 53, 1024–1035.
Malformations in North Sea pelagic fish embryos during the period 1984–1995.Crossref | GoogleScholarGoogle Scholar |

Dethlefsen, V., Westernhagen, H., Tüg, H., Hansen, P., and Dizer, H. (2001). Influence of solar ultraviolet-B on pelagic fish embryos: osmolality, mortality and viable hatch. Helgoland Marine Research 55, 45–55.
Influence of solar ultraviolet-B on pelagic fish embryos: osmolality, mortality and viable hatch.Crossref | GoogleScholarGoogle Scholar |

Dong, Q., Svoboda, K., Tiersch, T., and Monroe, T. (2007). Photobiological effects of UVA and UVB light in zebrafish embryos: evidence for a competent photorepair system. Journal of Photochemistry and Photobiology. B, Biology 88, 137–146.
Photobiological effects of UVA and UVB light in zebrafish embryos: evidence for a competent photorepair system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVCmt7rF&md5=5e373fc08b64154ba8ac7724de390377CAS | 17716904PubMed |

Fabra, M., Raldúa, D., Power, D., Deen, P., and Cerda, J. (2005). Marine fish egg hydration is aquaporin-mediated. Science 307, 545.
Marine fish egg hydration is aquaporin-mediated.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXosl2gtw%3D%3D&md5=19eeef9bc50f0164ebf1e8807dfb6e9dCAS | 15681377PubMed |

Farman, J., Gardiner, G., and Shanklin, J. (1985). Large losses of total ozone in Artarctica reveal seasonal CIOx/NOx interaction. Nature 315, 207–210.
Large losses of total ozone in Artarctica reveal seasonal CIOx/NOx interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktFSltrc%3D&md5=2a3724fcc5a49fdfb923b6c19cf5a9d1CAS |

Fukunishi, Y., Masuda, R., and Yamashita, Y. (2010). Exposure of eggs to solar UV-B leads to reduced hatching rates in two sparid fishes, red sea bream Pagrus major and black sea bream Acanthopagrus schlegel. Journal of Fish Biology 76, 734–741.
Exposure of eggs to solar UV-B leads to reduced hatching rates in two sparid fishes, red sea bream Pagrus major and black sea bream Acanthopagrus schlegel.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cjhtVSlug%3D%3D&md5=bafa7b7fcf5860771611051a2ebc7e99CAS | 20666911PubMed |

Fukunishi, Y., Browman, H., Durif, C., Bjelland, R., Shema, S., Fields, D., and Skiftesvik, A. (2013). Sub-lethal exposure to ultraviolet radiation reduces prey consumption by Atlantic cod larvae (Gadus morhua). Marine Biology 160, 2591–2596.
Sub-lethal exposure to ultraviolet radiation reduces prey consumption by Atlantic cod larvae (Gadus morhua).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFGjsL%2FO&md5=e2510449287c40bd43b4120cb9efb99eCAS |

Giraud, N. (2011). Distribución vertical de huevos de Engraulis ringens (Jenyns, 1842) en el fiordo de Reloncaví, X Región, Chile. M.Sc. dissertation, University of Concepción.

Häder, D., Kumar, H., Smith, R., and Worrest, R. (2007). Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochemical & Photobiological Sciences 6, 267–285.
Effects of solar UV radiation on aquatic ecosystems and interactions with climate change.Crossref | GoogleScholarGoogle Scholar |

Hernández, K., Quiñones, R., Daneri, G., and Helbling, E. (2006). Effects of solar radiation on bacterioplankton production in the upwelling system off central-southern Chile. Marine Ecology Progress Series 315, 19–31.
Effects of solar radiation on bacterioplankton production in the upwelling system off central-southern Chile.Crossref | GoogleScholarGoogle Scholar |

Herrera, G., Tarifeño, E., and Orellana, M. (1987). Descripción de huevos y primeras fases larvales de la sardina común (Strangomera bentincki) y del machuelo (Ethmidium maculatum). Biología Pesquera 16, 107–113.

Huff, D., Grad, G., and Williamson, C. E. (2004). Environmental constraints on spawning depth of yellow perch: the roles of low temperature and high solar ultraviolet radiation. Transactions of the American Fisheries Society 133, 718–726.
Environmental constraints on spawning depth of yellow perch: the roles of low temperature and high solar ultraviolet radiation.Crossref | GoogleScholarGoogle Scholar |

Hunter, J., Kaupp, R., and Taylor, J. (1981). Effects of solar and artificial ultraviolet-B radiation on larval northen anchovy, Engraulis mordax. Photochemistry and Photobiology 34, 477–486.
Effects of solar and artificial ultraviolet-B radiation on larval northen anchovy, Engraulis mordax.Crossref | GoogleScholarGoogle Scholar |

Huret, M., Runge, J., Chen, C., Cowles, G., Xu, Q., and Pringle, J. (2007). Dispersal modeling of fish early life stages: sensitivity with application to Atlantic cod in the western Gulf of Maine. Marine Ecology Progress Series 347, 261–274.
Dispersal modeling of fish early life stages: sensitivity with application to Atlantic cod in the western Gulf of Maine.Crossref | GoogleScholarGoogle Scholar |

Kouwenberg, J., Browman, H., Cullen, J., Davis, R., St-Pierre, J., and Runge, J. (1999). Biological weighting of ultraviolet (280–400 nm) induced mortality in marine zooplankton and fish. I. Atlantic cod (Gadus morhua) eggs. Marine Biology 134, 269–284.
Biological weighting of ultraviolet (280–400 nm) induced mortality in marine zooplankton and fish. I. Atlantic cod (Gadus morhua) eggs.Crossref | GoogleScholarGoogle Scholar |

Krautz, M. C., Vásquez, S., Castro, L., González, M., Llanos-Rivera, A., and Pantoja, S. (2010). Changes in metabolic substrates during early development in anchoveta Engraulis ringens (Jenyns 1842) in the Humboldt Current. Marine Biology 157, 1137–1149.
Changes in metabolic substrates during early development in anchoveta Engraulis ringens (Jenyns 1842) in the Humboldt Current.Crossref | GoogleScholarGoogle Scholar |

Krautz, M. C., Castro, L., González, M., Llanos-Rivera, A., Montes, I., González, H., González, R., and Vera, J. (2013). Concentration of ascorbic acid and antioxidant response in early life stages of Engraulis ringens and zooplankton during the spawning seasons of 2006–2009 off central Chile. Marine Biology 160, 1177–1188.
Concentration of ascorbic acid and antioxidant response in early life stages of Engraulis ringens and zooplankton during the spawning seasons of 2006–2009 off central Chile.Crossref | GoogleScholarGoogle Scholar |

Kuhn, P., Browman, H., StPierre, J., and Mcarthur, B. (1999). Penetration of ultraviolet radiation in the waters of the estuary and Gulf of St Lawrence. Limnology and Oceanography 44, 710–716.
Penetration of ultraviolet radiation in the waters of the estuary and Gulf of St Lawrence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1yjsL8%3D&md5=8e064ba5223d7b9f928e61186c04aa59CAS |

Laurion, I., Vincent, W., and Lean, D. (1997). Underwater ultraviolet radiation: development of spectral models for northern high latitude lakes. Photochemistry and Photobiology 65, 107–114.
| 1:CAS:528:DyaK2sXls12nsQ%3D%3D&md5=2386d265fd5a91948561f510d08f673aCAS |

Lesser, M., Farrell, J., and Walker, C. (2001). Oxidative stress, DNA damage and p53 expression in the larvae of Atlantic cod (Gadus morhua) exposed to ultraviolet (290–400 nm) radiation. The Journal of Experimental Biology 204, 157–164.
| 1:CAS:528:DC%2BD3MXps1emtA%3D%3D&md5=c1c34276d43762b7a8272374f59a87abCAS | 11104719PubMed |

Llabrés, M., Agustí, S., Fernández, M., Canepa, A., Maurin, F., Vidal, F., and Duarte, C. (2013). Impact of elevated UVB radiation on marine biota: a meta-analysis. Global Ecology and Biogeography 22, 131–144.
Impact of elevated UVB radiation on marine biota: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Llanos-Rivera, A., and Castro, L. (2004). Latitudinal and seasonal egg size variation of the anchoveta Engraulis ringens, off the Chilean coast. Fishery Bulletin 102, 207–212.

Llanos-Rivera, A., Vásquez, P., and Castro, L. (2013). Malformations in the embryonic development of Engraulis ringens (Clupeiformes) in a spawning area off central-southern Chile: description and rates. Journal of the Marine Biological Association of the United Kingdom 93, 2225–2234.
Malformations in the embryonic development of Engraulis ringens (Clupeiformes) in a spawning area off central-southern Chile: description and rates.Crossref | GoogleScholarGoogle Scholar |

Madronich, S. (1994). Increases in biologically damaging UV-B radiation due to stratospheric ozone reductions: a brief review. Ergebnisse der Limnologie 43, 17–30.

Mangor-Jensen, A., and Waiwood, K. (1995). The effect of light exposure on buoyancy of halibut eggs. Journal of Fish Biology 47, 18–25.
The effect of light exposure on buoyancy of halibut eggs.Crossref | GoogleScholarGoogle Scholar |

Moser, H., and Ahlstrom, E. (1985). Staging anchovy eggs. In ‘An Egg Production Method for Estimating Spawning Biomass of Pelagic Fish: Application to the Northern Anchovy, Engraulis mordax’. (Ed. R. Lasker.) NOAA Technical Report NMFS 36, pp. 37–41. (US Department of Commerce: La Jolla, CA.)

Ospina-Álvarez, A., Palomera, I., and Parada, C. (2012). Changes in egg buoyancy during development and its effects on the vertical distribution of anchovy eggs. Fisheries Research 117–118, 86–95.
Changes in egg buoyancy during development and its effects on the vertical distribution of anchovy eggs.Crossref | GoogleScholarGoogle Scholar |

Plack, P., Fraser, N., Grant, P., Middleton, C., Mitchell, A., and Thomson, R. (1981). Gadusol, an enolic derivative of cyclohexane–1,3-dione present in the roes of cod and other marine fish. Isolation, properties and occurrence compared with ascorbic acid. The Biochemical Journal 199, 741–747.
| 1:CAS:528:DyaL38XkvFaktg%3D%3D&md5=6605427b1028d9624367c0041c60d829CAS | 7200360PubMed |

Rain-Franco, A., Muñoz, G., and Fernandez, C. (2014). Ammonium production off central Chile (36°S) by photodegradation of phytoplankton-derived and marine dissolved organic matter. PLOS ONE 9, e100224.
Ammonium production off central Chile (36°S) by photodegradation of phytoplankton-derived and marine dissolved organic matter.Crossref | GoogleScholarGoogle Scholar | 24968138PubMed |

Sancar, A., and Sancar, G. (1988). DNA repair enzymes. Annual Review of Biochemistry 57, 29–67.
DNA repair enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlt1Cksbs%3D&md5=41859c959a7760818bd0ddc01297623cCAS | 3052275PubMed |

Schreck, C., Contreras-Sanchez, W., and Fitzpatrick, M. (2001). Effects of stress on fish reproduction, gamete quality, and progeny. Aquaculture 197, 3–24.
Effects of stress on fish reproduction, gamete quality, and progeny.Crossref | GoogleScholarGoogle Scholar |

Sepúlveda, A., Cubillos, L., Nuñez, S., Canales, T., Bucarey, D., and Rojas, A. (2000). Antecedentes biológicos del stock desovante de anchoveta y sardina común de la V y IX regiones. Informe Final Project Report FIP 97-04. Instituto de Investigación Pesquera, Valparaíso, Chile.

Steeger, H., Freitag, J., Michl, S., Wiemer, M., and Paul, R. (2001). Effects of UV-B radiation on embryonic, larval and juvenile stages of North Sea plaice (Pleuronectes platessa) under simulated ozone-hole conditions. Helgoland Marine Research 55, 56–66.
Effects of UV-B radiation on embryonic, larval and juvenile stages of North Sea plaice (Pleuronectes platessa) under simulated ozone-hole conditions.Crossref | GoogleScholarGoogle Scholar |

Strähle, U., and Jesuthasan, S. (1993). Ultraviolet irradiation impairs epiboly in zebrafish embryos: evidence for a microtubule-dependent mechanism of epiboly. Development 119, 909–919.
| 8187646PubMed |

Sundby, S. (1991). Factors affecting the vertical distribution of eggs. ICES Marine Science Symposia 192, 33–38.

Vásquez, P., Llanos-Rivera, A., and Castro, L. R. (2010). Anormalidades durante el desarrollo embrionario de sardina común, Strangomera bentincki en el ambiente natural. Revista de Biología Marina y Oceanografía 45, 177–185.
Anormalidades durante el desarrollo embrionario de sardina común, Strangomera bentincki en el ambiente natural.Crossref | GoogleScholarGoogle Scholar |

Vernet, M., Diaz, M., Fuenzalida, H., Camilion, C., Booth, C., Cabrera, S., Casiccia, C., Deferrari, G., Lovengreen, C., Paladini, H., Pedroni, J., Rosales, A., and Zagarese, H. (2009). Quality of UVR exposure for different biological systems along a latitudinal gradient. Photochemical & Photobiological Sciences 8, 1329–1345.
Quality of UVR exposure for different biological systems along a latitudinal gradient.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVGgs7bE&md5=40d8b1d1be5d7f9fbf9d556b92c1ff02CAS |

Vetter, R., Kurtzmann, A., and Mori, T. (1999). Diel cycles of DNA damage and repair in eggs and larvae of northern anchovy, Engraulis mordax, exposed to solar ultraviolet radiation. Photochemistry and Photobiology 69, 27–33.
Diel cycles of DNA damage and repair in eggs and larvae of northern anchovy, Engraulis mordax, exposed to solar ultraviolet radiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtlGrsw%3D%3D&md5=787f6c82a3fb6c6a727807b9666374afCAS |

Von Westernhagen, H. (1988). Sublethal effects of pollutants on fish eggs and larvae. In ‘Fish Physiology’. (Eds W. S. Hoar, and D. J. Randall.) pp. 253–346. (Academic Press: New York.)

Whitehead, R., de Mora, S., and Demers, S. (2004). Enhanced UV radiation – a new problem for the marine environment. In ‘The Effects of UV Radiation in the Marine Environment’. (Eds S. de Mora, S. Demers, and M. Vernet.) pp. 1–34. (Cambridge University Press: Cambridge, UK.)

Williamson, C., Neale, P., Grad, G., De Lange, H., and Hargreaves, B. (2001). Beneficial and detrimental effects of UV on aquatic organisms: implications of spectral variation. Ecological Applications 11, 1843–1857.
Beneficial and detrimental effects of UV on aquatic organisms: implications of spectral variation.Crossref | GoogleScholarGoogle Scholar |

Zagarese, H., and Williamson, C. (2004). Impact of solar UV radiation on zooplankton and fish. In ‘The Effects of UV Radiation in the Marine Environment’. (Eds S. de Mora, S. Demers, and M. Vernet.) pp. 279–309. (Cambridge University Press: Cambridge, UK.)