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Embryonic development of eggs and stereological analysis of body of Neoechinorhynchus buttnerae (Golvan, 1956) (Eoacanthocephala: Neoechinorhynchidae)

Published online by Cambridge University Press:  02 November 2021

Mayra da Silva Gonçalves
Affiliation:
Laboratório de Sanidade de Animais Aquáticos, Departamento de Ciências Pesqueiras, Universidade Federal do Amazonas (UFAM), Manaus, AM, Brazil
Oscar Tadeu Ferreira da Costa
Affiliation:
Laboratório de Morfologia Quantitativa, Departamento de Morfologia, Universidade Federal do Amazonas (UFAM), Manaus, AM, Brazil
Germán Augusto Murrieta Morey
Affiliation:
Instituto de Investigaciones de la Amazonía Peruana (IIAP), Iquitos-Loreto, Peru
Lucas Castanhola Dias
Affiliation:
Laboratório Temático de Microscopia Ótica e Eletrônica, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, AM, Brazil
Edsandra Campos Chagas
Affiliation:
Embrapa Amazônia Ocidental, Manaus, AM, Brazil
Sanny Maria de Andrade Porto*
Affiliation:
Laboratório de Sanidade de Animais Aquáticos, Departamento de Ciências Pesqueiras, Universidade Federal do Amazonas (UFAM), Manaus, AM, Brazil
*
Author for correspondence: Sanny Maria de Andrade Porto, E-mail: [email protected]

Abstract

The egg is one of the fundamental parts of the life cycle of Neoechinorhynchus buttnerae, and this stage involves the acanthor larva. It is also the infection phase for the intermediate host. Under normal conditions, the larva inside the egg can survive for months in the environment; however, information regarding this phase of life of the parasite is scarce. In addition, there is no quantitative information about the structural composition of the parasite's body from a histological point of view. Such information is essential in order to support decisions aimed at controlling infestations by these parasites in fish farming. This study aimed to present a detailed description of the stages of embryonic development of N. buttnerae eggs, as well as a stereological evaluation of the body of adult females of the parasite. Three phases of development characterized the eggs: cell division (with four stages), formation of the internal nuclear mass (with four stages) and formation of the acanthor larva (with five stages). The ovary comprised 26.61% of the volume of the animal and most of it contained eggs (21.28%), ovarian balls (3.88%) and empty spaces (1.45%). These results are of great importance and will support future studies that seek to interrupt the life cycle of this parasite.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Al-Sady, RS (2009) The life cycle and larval development of Neoechinorhynchus iraqensis (Acanthocephala: Neoechinorhynchidae) in the intermediate host. Ibn AL-Haitham Journal for Pure and Applied Science 22, 2.Google Scholar
Amin, OM (1987) Key to the families and subfamilies of acanthocephala with the erection of a new class (Polyacanthocephala) and a new order (Polyacanthorhynchida). Journal of Parasitology 73, 12161219.CrossRefGoogle Scholar
Anantaraman, S and Ravindranath, MH (1976) Histochemical characteristics of the egg envelopes of Acanthosentis sp. (Acanthocephala). Zeitschrift für Parasitenkunde 48, 227238.10.1007/BF00380396CrossRefGoogle Scholar
Anantaraman, S and Subramoniam, T (1975) Oogenesis in Acanthosentis oligospinus n.sp., an acanthocephalan parasite of the fish, Macrones gulio. Proceedings of the Indian Academy of Sciences-Section B 82, 139145.CrossRefGoogle Scholar
Awachie, JBE (1966) The development and life history of Echinorhynchus truttae Schrank, 1788 (Acanthocephala). Journal of Helminthology 40, 1132.10.1017/S0022149X00034040CrossRefGoogle Scholar
Castro, LA, Jerônimo, GT, Silva, RM, Santos, MJ, Ramos, CA and Andrade-Porto, SM (2020) Occurrence, pathogenicity, and control of acanthocephalosis caused by Neoechinorhynchus buttnerae: a review. Brazilian Journal of Veterinary Parasitology 29, e008320.Google ScholarPubMed
Cavalieri, B (1635) Geometria Indivisibilibus Continuorum Nova Quadam Ratione Promota, 1st Edn. Bologna, v. 1635.Google Scholar
Conselho Nacional de Controle de Experimentação Animal (CONCEA) (2013) Diretriz brasileira para o cuidado a Utilização de Animais para fins científicos e didáticos –DBCA. Brasília/DF. Ministério da Ciência Tecnologia e Inovação, p. 50.Google Scholar
Crompton, DWT and Walters, DE (1972) An analysis of the course of infection of Moniliformis dubius (Acanthocephala) in rats. Parasitology 64, 517523.10.1017/S0031182000045583CrossRefGoogle ScholarPubMed
Crompton, DWT and Whitfield, PJ (1968) The course of infection and egg production of Polymorphus minutus (Acanthocephala) in domestic ducks. Parasitology 58, 231246.10.1017/S0031182000073583CrossRefGoogle Scholar
Crompton, DWT and Whitfield, PJ (1974) Observations on the functional organization of the ovarian balls of Moniliformis and Polymorphus (Acanthocephala). Parasitology 69, 429443.10.1017/S0031182000063101CrossRefGoogle Scholar
Crompton, DWT, Arnold, S and Walters, DE (1976) The number and size of ovarian balls of Moniliformis (Acanthocephala) from laboratory rats. Parasitology 73, 6572.10.1017/S0031182000051337CrossRefGoogle ScholarPubMed
Cruz-Orive, LM (1999) Precision of Cavalieri sections and slices with local errors. Journal of Microscopy 193, 182198.CrossRefGoogle ScholarPubMed
Cuvier, G (1816) Le Règne Animal Edition 1. v. 2: i-xviii + 1-532, (Pls. 9-10, in v. 4).Google Scholar
Felix, A and McGuire, EJ (1981) Quantitative stereology: toxicologic pathology applications. Toxicologic Pathology 9, 2128.Google Scholar
George, PV and Nadakal, AM (1973) Studies on the life cycle of Pallisentis nagpurensis Bhalerao, 1931 (Pallisentidae; Acanthocephala) parasitic in the fish Ophiocephalus striatus (Bloch). Hydrobiologia 42, 3143.CrossRefGoogle Scholar
Golvan, YJ (1956) Acanthocéphales d'Amazonie. Redescription d'Oligacanthorhynchus iheringi Travassos, 1916 et description de Neoechinorhynchus buttnerae n. sp. (Neoacanthocephala-Neoechinorhynchidae). Annales de Parasitologie 31, 500524.Google Scholar
Gundersen, H and Østerby, R (1981) Optimizing sampling efficiency of stereological studies in biology: or ‘Do more less well!’. Journal of Microscopy 121, 6573.10.1111/j.1365-2818.1981.tb01199.xCrossRefGoogle Scholar
Gundersen, HJG, Bagger, P, Bendtsen, TF, Evans, SM, Korbo, L, Marcussen, N, Møller, A, Nielsen, K, Nyengaard, JR, Pakkenberg, B, SØRensen, FB, Vesterby, A and West, MJ (1988a) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. Apmis 96, 857881.CrossRefGoogle Scholar
Gundersen, HJG, Bendtsen, TF, Korbo, L, Marcussen, N, Moller, A, Nilsen, K, Nyengaard, JR, Pakkenberg, B, Sorensen, FB, Vesterby, A and West, MJ (1988b) Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. Apmis 96, 379394.10.1111/j.1699-0463.1988.tb05320.xCrossRefGoogle Scholar
Hammer, Ø, Harper, DA and Ryan, PD (2001) Paleontological statistics software: package for education and data analysis. Palaeontologia Electronica 4, 9.Google Scholar
Hartlev, LB, Klose-Jensen, R, Thomsen, JS, Nyengaard, JR, Boel, LW, Laursen, MB, Laurberg, TB, Nielsen, AW, Steengaard-Pedersen, K and Hauge, E (2018) Thickness of the bone-cartilage unit in relation to osteoarthritis severity in the human hip joint. RMD Open 4, e000747.10.1136/rmdopen-2018-000747CrossRefGoogle ScholarPubMed
Hopp, WB (1954) Studies on the morphology and life cycle of Neoechinorhynchus emydis (Leidy), an acanthocephalan parasite of the map turtle, Graptemys geographica (Le Sueur). The Journal of Parasitology 40, 284299.10.2307/3273740CrossRefGoogle Scholar
Howard, CV and Reed, MG (2005) Unbiased Stereology: Three-Dimensional Measurement in Microscopy. New York, Berlin, Heidelberg: Springer-Verlag.Google Scholar
Kiernan, JA (1999) Histological and histochemical methods: theory and practice. Shock 12, 479.Google Scholar
Kremer, JR, Mastronarde, DN and McIntosh, JR (1996) Computer visualization of three-dimensional image data using IMOD. Journal of Structural Biology 116, 7176.CrossRefGoogle ScholarPubMed
Lourenço, F, Morey, GAM and Malta, J (2018) The development of Neoechinorhynchus buttnerae (Eoacanthocephala: Neoechinorhynchidae) in its intermediate host Cypridopsis vidua in Brazil. Acta Parasitologica 63, 354359.CrossRefGoogle ScholarPubMed
Mandarim-de-Lacerda, CA (2003) Stereological tools in biomedical research. Anais da Academia Brasileira de Ciências 75, 469486.CrossRefGoogle ScholarPubMed
Marchand, B (1984) A comparative ultrastructural study of the shell surrounding the mature acanthor larvae of 13 acanthocephalan species. The Journal of Parasitology 70, 886901.CrossRefGoogle Scholar
Merritt, SV and Pratt, I (1964) The life history of Neoechinorhynchus rutili and its development in the intermediate host (Acanthocephala: Neoechinorhynchidae). The Journal of Parasitology 50, 394400.CrossRefGoogle Scholar
Miller, DM and Dunagan, TT (1985) New aspects of acanthocephalan lacunar system as revealed in anatomical modeling by corrosion cast method. Journal of the Helminthological Society of Washington 52, 221226.Google Scholar
Nesheim, MC, Crompton, DWT, Arnold, S and Barnard, D (1978) Host dietary starch and Moniliformis (Acanthocephala) in growing rats. Proceedings of the Royal Society B: Biological Sciences 202, 399408.Google Scholar
Nicholas, WL (1967) The biology of the Acanthocephala. Advances in Parasitology 5, 205246.CrossRefGoogle ScholarPubMed
Nicholas, WL and Hynes, HBN (1963) The embryology of Polymorphus minutus (Acanthocephala). Proceedings of the Zoological Society of London 141, 791801.10.1111/j.1469-7998.1963.tb01626.xCrossRefGoogle Scholar
Nikishin, VP (2001) A estrutura e formação de envelopes embrionários em acantocéfalos. Biology Bulletin 28, 4053.10.1023/A:1026606704436CrossRefGoogle Scholar
Parshad, VR, Crompton, DWT and Nesheim, MC (1980) The growth of Moniliformis (Acanthocephala) in rats fed on various monosaccharides and disaccharides. Proceedings of the Royal Society of London. Series B. Biological Sciences 209, 299315.Google ScholarPubMed
Parshad, VR and Crompton, DWT (1982) Aspects of acanthocephalan reproduction. Advances in Parasitology 19, 73138.CrossRefGoogle Scholar
Parshad, VR and Guraya, SS (1977) Morphological and histochemical observations on the ovarian balls of Centrorhynchus corvi (Acanthocephala). Parasitology 74, 243253.CrossRefGoogle Scholar
Pfenning, AC and Sparkes, TC (2019) Egg fibrils and transmission in the acanthocephalan Acanthocephalus dirus. Parasitology Research 118, 12251229.10.1007/s00436-019-06251-8CrossRefGoogle ScholarPubMed
Poulin, R and Morand, S (2000) Tests size, body size and male–male competition in acanthocephalan parasites. Journal of Zoology 250, 551558.CrossRefGoogle Scholar
Sasal, P, Jobet, E, Faliex, E and Morand, S (2000) Sexual competition in an acanthocephalan parasite of fish. Parasitology 120, 6569.CrossRefGoogle Scholar
Schmidt, G (1973) Early embryology of the Acanthocephalan Mediorhynchus grandis Van Cleave, 1916. Transactions of the American Microscopical Society 92, 512516.CrossRefGoogle Scholar
Schmidt, GD and Nickol, BB (1985) Development and life cycles. In Crompton, DWT, and Nickol, BB (eds), Biology of the Acanthocephala. Copyright: Cambridge University Press.Google Scholar
Serra, BNV (2019) Óleos essenciais de Lippia spp. no controle do estágio inicial do acantocéfalo Neoechinorhynchus buttnerae, endohelminto de tambaqui Colossoma macropomum. Dissertação de mestrado. Florianópolis, Santa Catarina, Brasil.Google Scholar
Silva-Gomes, AL, Gomes, CFJ, Viana-Silva, W, Braga-Oliveira, MI, Bernardino, G and Costa, JI (2017) The impact of Neoechinorhynchus buttnerae (Golvan, 1956) (Eoacanthocephala: Neochinorhynchidae) outbreaks on productive and economic performance of the tambaqui Colossoma macropomum (Cuvier, 1818), reared in ponds. Latin American Journal of Aquatic Research 45, 496500.CrossRefGoogle Scholar
Thatcher, VE (2006) Amazon Fish Parasites, 2nd Edn. Sofia, Moscow: Pensoft Publishers.Google Scholar
Uglem, GL (1972) The life cycle of Neoechinorhynchus cristatus Lynch, 1936 (Acanthocephala) with notes on the hatching of eggs. The Journal of Parasitology 58, 10711074.10.2307/3278138CrossRefGoogle ScholarPubMed
Uglem, GL and Larson, OR (1969) The life history and larval development of Neoechinorhynchus saginatus Van Cleave and Bangham, 1949 (Acanthocephala: Neoechinorhynchidae). The Journal of Parasitology 55, 12121217.CrossRefGoogle Scholar
Uznanski, RL and Nickol, BB (1976) Structure and function of the fibrillar coat of Leptorhynchoides thecatus eggs. The Journal of Parasitology 62, 569573.CrossRefGoogle ScholarPubMed
Valladão, GMR, Gallani, SU, Jerônimo, GT and Seixas, ATD (2019) Challenges in the control of acanthocephalosis in aquaculture: special emphasis on Neoechinorhynchus buttnerae. Reviews in Aquaculture 1, 113.Google Scholar
Violante-González, J, Villalba-Vásquez, PJ, Monks, S, García-Ibáñez, S, Rojas-Herrera, AA and Flores-Garza, R (2016) Características reprodutivas do acantocochalan Neoechinorhynchus brentnickoli no hospedeiro definitivo. Invertebrate Biology 136, 514.CrossRefGoogle Scholar
Wharton, D (1983) The production and functional morphology of helminth egg-shells. Parasitology 86, 8597.CrossRefGoogle ScholarPubMed