Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-20T16:42:51.007Z Has data issue: false hasContentIssue false

Malformations in the embryonic development of Engraulis ringens (Clupeiformes) in a spawning area off central–southern Chile: description and rates

Published online by Cambridge University Press:  09 July 2013

Alejandra Llanos-Rivera*
Affiliation:
Programa de Investigación Marina de Excelencia (PIMEX-Nueva Aldea), Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile Unidad de Biotecnología Marina, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile
Paulina Vásquez
Affiliation:
Programa de Investigación Marina de Excelencia (PIMEX-Nueva Aldea), Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile Programa de Magíster en Ciencias, mención Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile
Leonardo R. Castro
Affiliation:
Programa de Investigación Marina de Excelencia (PIMEX-Nueva Aldea), Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile Laboratorio de Oceanografía Pesquera y Ecología Larval, Programa COPAS Sur Austral and Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile
*
Correspondence should be addressed to: A. Llanos-Rivera, Unidad de Biotecnología Marina, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile email: [email protected]

Abstract

Variations in the rate of embryonic malformations of the anchoveta Engraulis ringens in a spawning area off central–southern Chile were assessed. Eggs in stages of development subsequent to blastodisc formation were collected and preserved. Several severe malformations were identified and grouped by: (1) proliferation of disorganized tissue in early and late developmental stages; (2) irregular blastopore closure; and (3) notochordal deformation, of which the second had the highest incidence among the embryos. The average rate of malformation was 5.64%, a value close to that reported for other Clupeiformes and below the rate of 10%, indicating the influence of purely endogenous factors. The expected relationship between temperature variations and malformation rates was not observed, probably because the natural temperature range experienced by the embryos was above that at which severe malformation had previously been observed in the laboratory. The relationship between egg size and malformation rates over the spawning season was not determined; however, a relationship between egg size and malformation rates was detected among the samples from each sampling date, which suggests that malformations may be attributable to endogenous factors rather than to environmental factors acting directly on the eggs in the plankton.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Avery, T., Killen, S. and Hollinger, T. (2009) The relationship of embryonic development, mortality, hatching success, and larval quality to normal or abnormal early embryonic cleavage in Atlantic cod, Gadus morhua . Aquaculture 289, 265273.CrossRefGoogle Scholar
Bodammer, J. (1993) The teratological and pathological effects of contaminants on embryonic and larval fishes exposed as embryos: a brief review. American Fisheries Society Symposium 14, 7784.Google Scholar
Bunn, N., Fox, C. and Webb, T. (2000) A literature review of studies on fish egg mortality: implications for the estimation of spawning stock biomass by the annual egg production method. Science Series Technical Report 111, Cefas, Lowestoft.Google Scholar
Cameron, P. and Berg, J. (1992). Morphological and chromosomal aberrations during embryonic development in dab Limanda limanda . Marine Ecology Progress Series 91, 163169.CrossRefGoogle Scholar
Cameron, P., Berg, J., Dethlefsen, V. and von Westernhagen, H. (1992) Developmental defects in pelagic embryos of several flatfish species in the southern North Sea. Netherlands Journal of Sea Research 29, 239256.CrossRefGoogle Scholar
Cameron, P., Berg, J. and von Westernhagen, H. (1996) Biological effects monitoring of the North Sea employing fish embryological data. Environmental Monitoring and Assessment 40, 107124.CrossRefGoogle ScholarPubMed
Castro, L.R. and Hernández, E.H. (2000) Early life survival of the anchoveta Engraulis ringens off central Chile during the 1995 and 1996 winter spawning seasons. Transactions of the American Fisheries Society 129, 11071117.2.0.CO;2>CrossRefGoogle Scholar
Castro, L., Llanos, A., Blanco, J., Tarifeño, E., Escribano, R. and Landaeta, M. (2002) Influence of latitudinal variations in spawning habitat characteristics on the early life history traits of the anchoveta, Engraulis ringens, off northern and central Chile. GLOBEC Report 16, 4245.Google Scholar
Castro, L.R., Claramunt, G., Krautz, M.C., Llanos-Rivera, A. and Moreno, P. (2009) Egg trait variation in anchoveta Engraulis ringens: a maternal response to changing environmental conditions in contrasting spawning habitats. Marine Ecology Progress Series 381, 237248.CrossRefGoogle Scholar
Castro, L.R., Claramunt, G., González, H., Krautz, M.C., Llanos-Rivera, A., Méndez, J., Schneider, W. and Soto, S. (2010) Fatty acids in anchoveta eggs, Engraulis ringens, during two contrasting winter spawning seasons. Marine Ecology Progress Series 420, 193205.CrossRefGoogle Scholar
Cubillos, L., Bucarey, D. and Canales, M. (2002) Monthly abundance estimation for common sardine Strangomera bentincki and anchovy Engraulis ringens in the central–south Chile (34–40°S). Fisheries Research 57, 117130.CrossRefGoogle Scholar
Cubillos, L., Canales, M., Bucarey, D., Rojas, A. and Alarcón, R. (1999) Época reproductiva y talla media de primera madurez sexual de Strangomera bentincki y Engraulis ringens en el período 1993–1997, en la zona centro-sur de Chile. Investigaciones Marinas 27, 7385.CrossRefGoogle Scholar
Cubillos, L.A., Ruiz, P., Claramunt, G., Gacitúa, S., Núñez, S., Castro, L.R., Riquelme, K., Alarcón, C., Oyarzún, C. and Sepúlveda, A. (2007) Spawning, daily egg production, and spawning stock biomass estimation for common sardine (Strangomera bentincki) and anchovy (Engraulis ringens) off central southern Chile in 2002. Fisheries Research 86, 228240.CrossRefGoogle Scholar
De Ciechomski, J.D. (1966) Influence of some environmental factors upon the embryonic development of the Argentine anchovy Engraulis anchoita (Hubbs & Marini). Report of California Cooperative Oceanic Fisheries Investigations 11, 6771.Google Scholar
Dethlefsen, V., von Westernhagen, H. and Cameron, P. (1996) Malformations in North Sea pelagic fish embryos during the period 1984–1995. ICES Journal of Marine Science 53, 10241035.CrossRefGoogle Scholar
Fischer, W. (1958) Huevos, crías y primeras prelarvas de la ‘anchoveta’ (Engraulis ringens) Jenyns. Revista de Biología Marina 8, 111124.Google Scholar
Grauman, G. (1982) On the emergence of sprat and cod abnormal embryos in the open Baltic. ICES Document CM 1982/J:7. Copenhagen: ICES Baltic Fish Committee.Google Scholar
Hammer, Ø., Harper, D. and Ryan, P. (2001) PAST: Paleontological Statistics software package for education and data analysis. Paleontologia Electronica 4(1).Google Scholar
Iriarte, J., Vargas, C., Tapia, F., Bermúdez, R. and Urrutia, R. (2012). Primary production and plankton carbon biomass in a river-influenced upwelling area off Concepción, Chile. Progress in Oceanography 9295, 97–109.Google Scholar
Krautz, M., Castro, L., González, M., Llanos-Rivera, A., Montes, I., González, H., González, R.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, 11771188.CrossRefGoogle Scholar
Klinger, R.C. and Van den Avyle, M. (1993) Preservation of striped bass eggs: effects of formalin concentration, buffering, stain, and initial stage of development. Copeia 1993, 11141119.CrossRefGoogle Scholar
Klumpp, D. and von Westernhagen, H. (1995) Biological effects of pollutants in Australian tropical coastal waters: embryonic malformations and chromosomal aberrations in developing fish eggs. Marine Pollution Bulletin 30, 158165.CrossRefGoogle Scholar
Klumpp, D., Humphrey, C., Huasheng, H. and Tao, F. (2002) Toxic contaminants and their biological effects in coastal waters of Xiamen, China. II. Biomarkers and embryo malformation rates as indicators of pollution stress in fish. Marine Pollution Bulletin 44, 761769.CrossRefGoogle Scholar
Koo, T. and Johnston, M. (1978) Larval deformity in striped bass, Morone saxatilis (Walbaum), and blueback herring, Alosa aestialis (Mitchell), due to heat shock treatment of developing eggs. Environmental Pollution 16, 137149.Google Scholar
Kunz, Y. (2004) Developmental biology of teleost fishes. Fish and Fisheries Series. New York: Springer.CrossRefGoogle Scholar
Leal, E., Castro, L. and Claramunt, G. (2009). Variability in oocyte size and batch fecundity of two anchovy stocks (Engraulis ringens, Jenyns 1842) off the Chilean coast. Scientia Marina 73, 5966.Google 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, 207212.Google Scholar
Llanos-Rivera, A. and Castro, L. (2006) Inter-population differences in temperature effects on Engraulis ringens yolk-sac larvae. Marine Ecology Progress Series 312, 245253.CrossRefGoogle Scholar
Makhotin, V., Solemdal, P., Korsbrekke, K. and Salthaug, A. (2001) Types and frequency of malformations and mortality in eggs of Arcto-Norwegian cod: a field study. Copenhagen: ICES, CM 2001/N:12.Google Scholar
Moser, H. and Ahlstrom, E. (1985) Staging anchovy eggs. In Moser, H. and Ahlstrom, E. (eds) An egg production method for estimating spawning biomass of pelagic fish: application to the northern anchovy, Engraulis mordax . NOAA Technical Report, NMFS 36, pp. 3741.Google Scholar
Serra, R., Aguayo, M., Rojas, O., Cañón, J. and Inostroza, F. (1979) Anchoveta Engraulis ringens (Jenyns) y Sardina común Clupea (Strangomera) bentincki . In Estado actual de las principales pesquerías nacionales. Bases para un desarrollo pesquero. Valparaiso: Instituto de Fomento Pesquero.Google Scholar
Schreck, C., Contreras-Sanchez, W. and Fitzpatrick, M. (2001) Effects of stress on fish reproduction, gamete quality, and progeny. Aquaculture 197, 324.CrossRefGoogle Scholar
StatSoft Inc. (2004) STATISTICA (data analysis software system), version 7. Available at: www.statsoft.com (accessed 5 June 2013).Google Scholar
Tarifeño, E., Carmona, M., Llanos-Rivera, A. and Castro, L. (2008) Temperature effect on development of anchoveta's egg: does latitudinal difference occur? Environmental Biology of Fishes 81, 387395.CrossRefGoogle Scholar
Von Westernhagen, H. (1970) Erbrütung der eier von dorsch (Gadus morhua), flunder (Pleuronectes flesus) und scholle (Pleuronectes platessa) unter kombinierten temperatur- und salzgehalts-bedingungen. Helgolander Wissenschaftliche Meeresuntersuchungen 21, 21102.CrossRefGoogle Scholar
Von Westernhagen, H. (1988) Sublethal effects of pollutants on fish eggs and larvae. In Hoar, W. and Randall, D.J. (eds) The physiology of developing fish. Academic Press: New York, pp. 253346.CrossRefGoogle Scholar
Von Westernhagen, H. and Dethlefsen, V. (1997) The use of malformations in pelagic fish embryos for pollution assessment. Hydrobiologia 352, 241250.CrossRefGoogle Scholar
Von Westernhagen, H., Dethlefsen, V. and Haarich, M. (2001) Can a pollution event be detected using a single biological effects monitoring method? Marine Pollution Bulletin 42, 294297.CrossRefGoogle ScholarPubMed
Wiegand, M., Hataley, J., Kitchen, C. and Buchanan, L. (1989) Induction of developmental abnormalities in larval goldfish, Carassius auratus L., under cool incubations. Journal of Fish Biology 35, 8595.CrossRefGoogle Scholar
Yannopoulos, A. and Yannopoulos, C. (1981) Fish egg mortality and abnormal embryogenesis. Rapports et Procès-Verbaux des Rèunions Commission Internationale pour l'Exploration de la Mer 27, 143146.Google Scholar