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Comparative Analysis of Spermatozoa Morphology in Three Fish Species from the Suborder Scorpaenoidei

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Abstract

The methods of scanning and transmission electron microscopy are used for the investigation of external morphology and ultrastructure of spermatozoa in scorpaenoid fishes Parascorpaena picta, Dendrochirus zebra (Scorpaenidae), and Synanceia horrida (Synanceiidae). Based on the literature data, a comparison with other species of the genera Scorpaena, Sebastapistes, and Scorpaenopsis (Scorpaenidae) is conducted. In the studied species, the spermatozoon consists of the rounded head (its length is slightly smaller than its width), moderately developed midpiece, and flagellum. P. picta differs from the other species in the presence of the widening of the cytoplasmic channel surrounding the initial part of the flagellum, the largest numbers of mitochondrial sections, and the longest flagellum. S. horrida does not differ significantly from the representatives of the family Scorpaenidae. However, based on the contour of the head and midpiece (elliptic Fourier analysis), there is a trend to the separation of S. horrida from P. picta and D. zebra. The data on comparative spermatozoa morphology are discussed in relation to current phylogenetic schemes.

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References

  • Abe, T. and Munehara, H., Adaptation and evolution of reproductive mode in copulating cottoid species, in Reproductive Biology and Phylogeny of Fishes, Jamieson, B.G.M., Ed., Enfield, NH: Sci. Publ., 2009, vol. 8, pp. 221–246.

    Google Scholar 

  • Arculeo, M. and Lo Brutto, S., New contribution to the systematic status of various Mediterranean scorpionfish, as inferred from a mitochondrial DNA sequence, Rev. Biol. Mar. Oceanogr., 2014, vol. 49, no. 2, pp. 367–371.

    Article  Google Scholar 

  • Baccetti, B. and Afzelius, B.A., The biology of the sperm cell, Monogr. Dev. Biol., 1976, vol. 10, pp. 1–254.

    Google Scholar 

  • Biagi, F., Piras, F., Farina, V., et al., Testis, structure, spermatogenesis and sperm morphology in pipefishes of the genus Syngnathus, Acta Zool. (Stockholm), 2016, vol. 97, pp. 90–101.

    Article  Google Scholar 

  • Bilecenoğlu, M., First sighting of the Red Sea originated stonefish (Synanceia verrucosa) from Turkey, J. Black Sea/Mediterr. Environ., 2012, vol. 18, no. 1, pp. 76–82.

    Google Scholar 

  • Burnett, J.W., Aquatic adversaries: stonefish, Cutis, 1998, vol. 62, pp. 269–270.

    PubMed  CAS  Google Scholar 

  • Burns, J.R. and Weitzman, S.H., Insemination in ostariophysan fishes, in Viviparous Fishes, Uribe, M.C. and Grier, H.J., Eds., Homestead: New Life, 2005, pp. 107–134.

    Google Scholar 

  • Burns, J.R., Weitzman, S.H., Grier, H., and Menezes, N.A., Internal fertilization, testis and sperm morphology in glandulocaudine fishes (Teleostei: Characidae: Glandulocaudinae), J. Morphol., 1995, vol. 224, pp. 131–145.

    Article  PubMed  Google Scholar 

  • Chuang, P. and Shiao, J., Toxin gene determination and evolution in scorpaenoid fish, Toxicon, 2014, vol. 88, pp. 21–33.

    Article  PubMed  CAS  Google Scholar 

  • Catalog of Fishes, California Academy of Sciences, Version 12/2016, Eschmeyer, W.N., Fricke, R., and Laan van der, R., Eds., 2016. http://www.calacademy.org/scientists/projects/catalog-of-fishes.

  • Emel’yanova, N.G. and Makeeva, A.P., Ultrastructure of spermatozoa of some carp (Cyprinidae) fishes, Vopr. Ikhtiol., 1985, vol. 25, no. 3, pp. 459–468.

    Google Scholar 

  • Emel’yanova, N.G. and Pavlov, D.A., Gamete ultrastructure in some species of the family Mullidae from the South China Sea, J. Ichthyol., 2012, vol. 52, no. 9, pp. 639–645.

    Article  Google Scholar 

  • Emel’yanova, N.G. and Pavlov, D.A., Gamete ultrastructure in two species of the genus Upeneus (Mullidae) from the South China Sea, J. Ichthyol., 2014, vol. 54, no. 4, pp. 286–292.

    Article  Google Scholar 

  • FAO Species Identification Guide for Fishery Purposes, The Living Marine Resources of the Western Central Pacific, Vol. 4: Bony Fishes, Part 2: Mugilidae to Carangidae, Carpenter, K.E. and Niem, V.H., Eds., Rome: Food Agric. Org., 1999, pp. 2069–2790.

  • FishBase, Version 10/2017, Froese, R. and Pauly, D., Eds., 2017. http://www.fishbase.org.

  • Fewings, D.G. and Squire, L.C., Notes on the reproduction in estuarine stonefish Synanceia horrida, SPC Live Reef Fish Info. Bull., 1999, vol. 5, pp. 31–33.

    Google Scholar 

  • Franzen, A., Sperm structure with regard to fertilization biology and phylogenetics, Verh. Dtsch. Zool. Ges., 1977, pp. 123–138.

    Google Scholar 

  • Frehlick, L.J., Eirín-López, J.M., Prado, A., et al., Sperm nuclear basic proteins of two closely related species of Scorpaeniform fish (Sebastes maliger, Sebastolobus sp.) with different sexual reproduction and the evolution of fish protamines, J. Exp. Zool., Part A, 2006, vol. 305, pp. 277–287.

    Google Scholar 

  • Ginzburg, A.S., Fertilization in Fishes and the Problem of Polyspermy, Jerusalem: Israel Program for Scientiic Translations, 1972.

    Google Scholar 

  • Giora, J. and Burns, J.R., Sperm ultrastructure in three different families of weakly electric fishes (Teleostei: Gymnotiformes), Neotrop. Ichthyol., 2011, vol. 9, no. 4, pp. 881–888.

    Article  Google Scholar 

  • Gwo, J.C., Yang, W.T., Kuo, M.C., et al., Spermatozoal ultrastructures of two marine perciform teleost fishes, the goatfish, Paraupeneus spilurus (Mullidae) and the rabbitfish, Siganus fuscescens (Siganidae) from Taiwan, Tissue Cell, 2004, vol. 36, pp. 63–69.

    Google Scholar 

  • Hammer, Ø., Harper, D.A.T., and Ryan, P.D., PAST: paleontological statistics software package for education and data analysis, Palaeontol. Electron., 2001, vol. 4, no. 1, pp. 1–9.

    Google Scholar 

  • Imamura, H., Phylogenetic relationships and new classification of the superfamily Scorpaenoidea (Actinopterygii: Perciformes), Species Div., 2004, vol. 9, pp. 1–36.

    Article  Google Scholar 

  • Ishida, M., Phylogeny of the suborder Scorpaenoidei (Pisces: Scorpaeniformes), Bull. Nansei Nat. Fish. Res. Inst., 1994, vol. 27, pp. 1–112.

    Google Scholar 

  • Iwata, H. and Ukai, Y., Shape: a computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors, J. Hered., 2002, vol. 93, pp. 384–385.

    Article  PubMed  CAS  Google Scholar 

  • Jamieson, B.G.M., Fish Evolution and Systematics: Evidence from Spermatozoa, Cambridge: Cambridge Univ. Press, 1991.

    Google Scholar 

  • Kime, D.E. and Tveiten, H., Unusual motility characteristics of sperm of the spotted wolfish, J. Fish Biol., 2002, vol. 61, no. 6, pp. 1549–1559.

    Article  Google Scholar 

  • Kochzius, M., Söller, R., Khalaf, M.A., and Blohm, D., Molecular phylogeny of the lion fish genera Dendrochirus and Pterois (Scorpaenidae, Pteroinae) based on mitochondrial DNA sequences, Mol. Phylogenet. Evol., 2003, vol. 28, pp. 396–403.

    Article  PubMed  CAS  Google Scholar 

  • Koya, Y. and Muñoz, M., Comparative study on ovarian structures in scorpaenids: possible evolutional process of reproductive mode, Ichthyol. Res., 2007, vol. 54, pp. 221–230.

    Article  Google Scholar 

  • Koya, Y., Hayakawa, Y., Markevich, A., and Munehara, H., Comparative studies of testicular structure and sperm morphology among copulatory and non-copulatory sculpins (Cottidae: Scorpaeniformes: Teleostei), Ichthyol. Res., 2011, vol. 58, pp. 109–125.

    Article  Google Scholar 

  • Kuhl, F.P. and Giardina, C.R., Elliptic Fourier features of a closed contour, Comput. Graph. Image Process., 1982, vol. 18, pp. 236–258.

    Article  Google Scholar 

  • Kwik, J.T.B., The biology and ecology of small tropical scorpaenoids inhabiting shallow coastal habitats in Singapore, PhD Thesis, Singapore: Natl. Univ. Singapore, 2011. http://scholarbank.nus.sg/handle/10635/31654.

    Google Scholar 

  • Lahnsteiner, F. and Patzner, R.A., Fine structure of spermatozoa of two marine teleost fishes, the red mullet, Mullus barbatus (Mullidae) and the white sea bream, Diplodus sargus (Sparidae), J. Submicrosc. Cytol. Pathol., 1995, vol. 27, pp. 259–266.

    Google Scholar 

  • Love, M.S., Yoklavich, M., and Thorsteinson, L., The Rock-Fishes of the Northeast Pacific, Berkeley: Univ. Calif. Press, 2002.

    Google Scholar 

  • Makeeva, A.P., Embriologiya ryb (Embryology of Fishes), Moscow: Mosk. Gos. Univ., 1992.

    Google Scholar 

  • Mattei, X., Spermatozoon ultrastructure and its systematic implication in fishes, Can. J. Zool., 1991, vol. 69, pp. 3038–3055.

    Article  Google Scholar 

  • Morris, J.A., Akins, J.L., Barse, A., et al., Biology and ecology of the invasive lionfishes, Pterois miles and Pterois volitans, Proc. 61st Gulf and Caribbean Fisheries Institute, Gosier, 2009, pp. 409–414.

    Google Scholar 

  • Moyer, J.T. and Zaiser, M.J., Social organization and spawning behavior of the Pteroine fish Dendrochirus zebra at Miyake-Jima, Japan, Jpn. J. Ichthyol., 1981, vol. 28, pp. 52–69.

    Google Scholar 

  • Munehara, H., Takano, K., and Koya, Y., Internal gametic association and external fertilization in the elkhorn sculpin, Alcichthys alcicornis, Copeia, 1989, no. 3, pp. 673–678.

    Article  Google Scholar 

  • Munehara, H., Koya, Y., and Takano, K., The little dragon sculpin Blepsias cirrhosus, another case of internal gametic association and external fertilization, Jpn. J. Ichthyol., 1991, vol. 37, pp. 391–397.

    Google Scholar 

  • Munehara, H., Koya, Y., Hayakawa, Y., and Takani, K., Extracellular environments for the initiation of external fertilization and micropylar plug formation in a cottid species, Hemitripterus villosus (Pallas) (Scorpaeniformes) with internal insemination, J. Exp. Mar. Biol. Ecol., 1997, vol. 211, pp. 279–289.

    Google Scholar 

  • Muñoz, M., Reproduction in Scorpaeniformes, in Reproduction and Sexuality in Marine Fishes: Patterns and Processes, Cole, K.S., Ed., Berkeley: Univ. Calif. Press, 2010, pp. 65–87.

    Google Scholar 

  • Muñoz, M., Casadevall, M., and Bonet, S., Testicular structure and semicystic spermatogenesis in a specialized ovuliparous species: Scorpaena notata (Pisces, Scorpaenidae), Acta Zool., 2002, vol. 83, no. 3, pp. 213–219.

    Article  Google Scholar 

  • Nozaki, R., Takushima, M., Mizuno, K., et al., Reproductive cycle of devil stinger, Inimicus japonicus, Fish Physiol. Biochem., 2003, vol. 28, pp. 217–218.

    Article  CAS  Google Scholar 

  • Pavlov, D.A., Differentiation of three species of the genus Upeneus (Mullidae) based on otolith shape analysis, J. Ichthyol., 2016, vol. 56, no. 1, pp. 37–51.

    Article  Google Scholar 

  • Pavlov, D.A. and Emel’yanova, N.G., Features of reproductive biology in two tropical fish species from the family Scorpaenidae, J. Ichthyol., 2007, vol. 47, no. 5, pp. 353–365.

    Article  Google Scholar 

  • Pavlov, D.A. and Emel’yanova, N.G., Reproductive biology of species from the family Scorpaenidae and transition from oviparity to viviparity in the southern and northern Percomorpha, in Viviparous Fishes II, Uribe, M.C. and Grier, H.J., Eds., Homestead: New Life, 2010, pp. 89–105.

    Google Scholar 

  • Pavlov, D.A. and Emel’yanova, N.G., Transition to viviparity in the order Scorpaeniformes: brief review, J. Ichthyol., 2013, vol. 53, no. 1, pp. 52–69.

    Article  Google Scholar 

  • Pavlov, D.A., Knudsen, P., Emel’yanova, N.G., and Moksness, E., Spernatozoon ultrastructure and sperm production in wolfish (Anarhichas lupus), a species with internal fertilization, Aquat. Living Resour., 1997, vol. 10, pp. 187–194.

    Article  Google Scholar 

  • Pusack, T.J., Benkwitt, C.F., Cure, K., and Kindinger, T.L., Invasive red lionfish (Pterois volitans) grow faster in the Atlantic Ocean than in their native Pacific range, Environ. Biol. Fish., 2016, vol. 99, pp. 571–579.

    Article  Google Scholar 

  • Rocha, L.A., Rocha, C.R., Baldwin, C.C., et al., Invasive lionfish preying on critically endangered reef fish, Coral Reefs, 2015, vol. 34, pp. 803–806.

    Article  Google Scholar 

  • Sàbat, M., Lo Nostro, F., Casadevall, M., and Muñoz, M., A light and electron microscopic study on the organization of the testis and the semicystic spermatogenesis of the genus Scorpaena (Teleostei, Scorpaenidae), J. Morphol., 2009, vol. 270, pp. 662–672.

    Article  PubMed  Google Scholar 

  • Smith, W.L. and Busby, M.S., Phylogeny and taxonomy of sculpins, sandfishes, and snailfishes (Perciformes: Cottoidei) with comments on the phylogenetic significance of their early-life-history specializations, Mol. Phylogenet. Evol., 2014, vol. 79, pp. 332–352.

    Article  PubMed  Google Scholar 

  • Smith, W.L. and Wheeler, W.C., Polyphyly of the mailcheeked fishes (Teleostei: Scorpaeniformes): evidence from mitochondrial and nuclear sequence data, Mol. Phylogenet. Evol., 2004, vol. 32, pp. 627–646.

    Article  PubMed  CAS  Google Scholar 

  • Spadella, M.A., Oliveira, C., and Quagio-Grassiotto, I., Comparative analysis of spermiogenesis and sperm ultrastructure in Callichthyidae (Teleostei: Ostariophysi: Siluriformes), Neotrop. Ichthyol., 2007, vol. 5, no. 3, pp. 337–350.

    Article  Google Scholar 

  • Turdakov, A.F., Vosproizvoditel’naya sistema samtsov ryb (Reproductive System of Fish Males), Frunze: Ilim, 1972.

    Google Scholar 

  • Vila, S., Munoz, M., Sabat, M., and Casadevall, M., Annual cycle of stored spermatozoa within the ovaries of Helicolenus dactylopterus dactylopterus (Teleostei, Scorpaenidae), J. Fish Biol., 2007, vol. 71, pp. 596–609.

    Article  Google Scholar 

  • Vila, S., Sàbat, M., Muñoz, M., and Casadevall, M., Spermiogenesis particularities of a sperm storage species: Helicolenus dactylopterus (Teleostei: Scorpaenidae), Sci. Mar., 2010, vol. 74, no. 4, pp. 687–704.

    Article  Google Scholar 

  • Wang, Y., Li, L., Cui, G., and Lu, W., Ontogenesis from embryo to juvenile and salinity tolerance of Japanese devil stinger Inimicus japonicus during early life stage, Springer-Plus, 2013, vol. 2, no. 289, pp. 1–13.

    CAS  Google Scholar 

  • Watanabe, K., Maturation of wild and reared female devil stinger, Inimicus japonicus, Aquacult. Sci., 2006, vol. 54, no. 4, pp. 495–503.

    Google Scholar 

  • Weakley, B.S., Beginner’s Handbook in Biological Electron Microscopy, Edinburgh: Churchill Livingstone, 1972.

    Google Scholar 

  • Wourms, J.P., Reproduction and development of Sebastes in the context of the evolution of piscine viviparity, Environ. Biol. Fish., 1991, vol. 30, pp. 111–126.

    Article  Google Scholar 

  • Wourms, J.P., Grove, B.D., and Lombardi, J., The maternal embryonic relationships in viviparous fishes, in Fish Physiology, Hoar, W.S. and Randall, D.J., Eds., San Diego: Academic, 1988, vol. 11, pp. 1–134.

    Google Scholar 

  • Yue, S., Estuarine stonefish Synanceia horrida (Linnaeus, 1766), 2015. https://taxo4254.wikispaces.com/synanceia+ horrida.

    Google Scholar 

  • Ziegman, R. and Alewood, P., Bioactive components in fish venoms, Toxins, 2015, vol. 7, pp. 1497–1531.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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  1. Biological Faculty, Moscow State University, Moscow, 119899, Russia

    D. A. Pavlov & N. G. Emel’yanova

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  1. D. A. Pavlov
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Correspondence to D. A. Pavlov.

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Original Russian Text © D.A. Pavlov, N.G. Emel’yanova, 2018, published in Voprosy Ikhtiologii, 2018, Vol. 58, No. 2, pp. 201–214.

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Pavlov, D.A., Emel’yanova, N.G. Comparative Analysis of Spermatozoa Morphology in Three Fish Species from the Suborder Scorpaenoidei. J. Ichthyol. 58, 226–238 (2018). https://doi.org/10.1134/S003294521802011X

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