The ultrastructure of spermatozoa in three species of cambarid crayfish, Cambarus robustus, Orconectes propinquus, and Orconectes rusticus, were studied and compared with eight previously studied species from different crayfish families using morphological features and biometrical data. The ultrastructure of spermatozoa show a generally conserved pattern including an acrosome and nucleus in the anterior and posterior parts of the cell, respectively, radial arms that wrap around the nucleus, and the whole cell is enclosed by an extracellular capsule. The most outstanding morphological feature in spermatozoa of three studied cambarid crayfish is the crest-like protrusions in the anterior part of the acrosome that can be used as one of the features for distinguishing the members of this family. Results of biometrical data reveal that acrosome size in the representatives of Parastacidae are the smallest, while representatives of Astacidae show the biggest acrosome. The acrosome size in species belonging to Cambaridae occupy an intermediate position between the two other families of freshwater crayfish. In conclusion, a combination of morphological features and biometrical data of spermatozoa can help distinguishing different species of the freshwater crayfish.

University of South Bohemia in České Budějovice Faculty of Fisheries and Protection of Waters South Bohemian Research Centre of Aquaculture and Biodiversity of Hydrocenoses Vodňany Czech Republic

Upper Canada College Toronto ON Canada

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Anderson WA, Ellis RA. Cytodifferentiation of the crayfish spermatozoon: acrosome formation, transformation of mitochondria and development of microtubules. Zeitschrift für Zellforschung und mikroskopische Anatomie. 1967;77:80–94. doi: 10.1007/bf00336700. PubMed DOI

André J. Contribution à la connaissance du chondriome. Journal of Ultrastructure Research. 1962;6:1–185. doi: 10.1016/S0889-1605(62)80002-0. PubMed DOI

Austin CM, Ryan SG. Allozyme evidence for a new species of freshwater crayfish of the genus Cherax Erichson (Decapoda: Parastacidae) from the south-west of Western Australia. Invertebrate Systematics. 2002;16:357–367. doi: 10.1071/IT01010. DOI

Beach D, Talbot P. Ultrastructural comparison of sperm from the crayfishes Cherax tenuimanus and Cherax albidus. Journal of Crustacean Biology. 1987;7:205–218. doi: 10.2307/1548602. DOI

Berrill M, Arsenault M. Spring breeding of a northern temperate crayfish, Orconectes rusticus. Canadian Journal of Zoology. 1982;60:2641–2645. doi: 10.1139/z82-339. DOI

Braga A, Nakayama CL, Poersch L, Wasielesky W. Unistellate spermatozoa of decapods: comparative evaluation and evolution of the morphology. Zoomorphology. 2013;132:261–284. doi: 10.1007/s00435-013-0187-2. DOI

Crandall KA, Buhay JE. Global diversity of crayfish (Astacidae, Cambaridae, and Parastacidae—Decapoda) in freshwater. Hydrobiologia. 2007;595:295–301. doi: 10.1007/s10750-007-9120-3. DOI

Dong W-L, Hou C-C, Yang W-X. Mitochondrial prohibitin and its ubiquitination during crayfish Procambarus clarkii spermiogenesis. Cell and Tissue Research. 2014;359:679–692. doi: 10.1007/s00441-014-2044-0. PubMed DOI

Dudenhausen E, Talbot P. Spermiogenesis in the crayfish, Pacifastacus leniusculus [Abstract] Journal of Cell Biology. 1979;83:225a.

Dudenhausen EE, Talbot P. An ultrastructural analysis of mature sperm from the crayfish Pacifastacus leniusculus, Dana. International Journal of Invertebrate Reproduction and Development. 1982;5:149–159. doi: 10.1080/01651269.1982.10553464. DOI

Dudenhausen EE, Talbot P. An ultrastructural comparison of soft and hardened spermatophores from the crayfish Pacifastacus leniusculus Dana. Canadian Journal of Zoology. 1983;61:182–194. doi: 10.1139/z83-023. DOI

Eliakova G, Goriachkina V. Some features of the crayfish spermatocyte ultrastructure. International congress for electron microscopy, Kyoto, Japan; August 28th–September 4th, 1966.1966.

Felgenhauer B, Abele L. Morphological diversity of decapod spermatozoa Crustacean sexual biology. Columbia University Press; New York: 1991. pp. 322–341.

Hinsch GW. Junctional complexes between the sertoli cells in the testis of the crayfish, Procambarus paeninsulanus. Tissue and Cell. 1992;24:379–385. doi: 10.1016/0040-8166(92)90054-B. PubMed DOI

Hinsch GW. Ultrastructure of spermatogonia, spermatocytes, and sertoli cells in the testis of the crayfish, Procambarus paeninsulanus. Tissue and Cell. 1993a;25:737–742. doi: 10.1016/0040-8166(93)90054-O. PubMed DOI

Hinsch GW. The role of sertoli cells in spermatid maturation in the testis of the crayfish, Procambarus paeninsulanus. Tissue and Cell. 1993b;25:743–749. doi: 10.1016/0040-8166(93)90055-P. PubMed DOI

Jamieson BGM. Ultrastructure and phylogeny of crustacean spermatozoa. Memoirs of the Queensland Museum. 1991;31:109–142. doi: 10.1016/S0044-8486(01)00511-7. DOI

Jamieson BGM, Tudge CC. Crustacea–Decapoda reproductive biology of invertebrates. In: Jamieson BGM, editor. Progress in male gamete ultrastructure and phylogeny. vol. 9. 2000. pp. 1–95. Part C.

Jerry DR. Electrical stimulation of spermatophore extrusion in the freshwater yabby (Cherax destructor) Aquaculture. 2001;200:317–322. doi: 10.1016/S0044-8486(01)00511-7. DOI

Kaye GI, Pappas GD, Yasuzumi G, Yamamoto H. The distribution and form of the endoplasmic reticulum during spermatogenesis in the crayfish, Cambaroides japonicus. Zeitschrift für Zellforschung und mikroskopische Anatomie. 1961;53:159–171. doi: 10.1007/bf00339439. PubMed DOI

Klaus S, Brandis D. Evolution of sperm morphology in potamid freshwater crabs (Crustacea: Brachyura: Potamoidea) Zoological Journal of the Linnean Society. 2011;161:53–63. doi: 10.1111/j.1096-3642.2009.00625.x. DOI

Klaus S, Schubart CD, Brandis D. Ultrastructure of spermatozoa and spermatophores of old world freshwater crabs (Brachyura: Potamoidea: Gecarcinucidae, Potamidae, and Potamonautidae) Journal of Morphology. 2009;270:175–193. doi: 10.1002/jmor.10678. PubMed DOI

Kouba A, Niksirat H, Bláha M. Comparative ultrastructure of spermatozoa of the redclaw Cherax quadricarinatus and the yabby Cherax destructor (Decapoda, Parastacidae) Micron. 2015;69:56–61. doi: 10.1016/j.micron.2014.11.002. PubMed DOI

López-Camps J, Bargalló R, Bozzo MG, Durfort M, Fontarnau R. The spermatogenesis of crustaceans. VII. Review of spermatozoon of the crayfish Astacus astacus (Malacostraca, Decapoda, Macrura, Reptantia) Gamete Research. 1981;4:65–82. doi: 10.1002/mrd.1120040110. DOI

López Greco LS, Lo Nostro FL. Structural changes in the spermatophore of the freshwater ‘red claw’ crayfish Cherax quadricarinatus (Von Martens, 1898) (Decapoda, Parastacidae) Acta Zoologica. 2008;89:149–155. doi: 10.1111/j.1463-6395.2007.00303.x. DOI

López-Greco LS, Vazquez F, Rodríguez EM. Morphology of the male reproductive system and spermatophore formation in the freshwater ‘red claw’ crayfish Cherax quadricarinatus (Von Martens, 1898) (Decapoda, Parastacidae) Acta Zoologica. 2007;88:223–229. doi: 10.1111/j.1463-6395.2007.00269.x. DOI

Moses MJ. Spermiogenesis in the crayfish (Procambarus clarkii) I. Structural characterization of the mature sperm. Journal of Biophysical and Biochemical Cytology. 1961a;9:222–228. PubMed PMC

Moses MJ. Spermiogenesis in the crayfish (Procambarus clarkii). II. Description of stages. Journal of Biophysical and Biochemical Cytology. 1961b;10:301–333. PubMed PMC

Niksirat H, Andersson L, James P, Kouba A, Kozák P. Proteomic profiling of the signal crayfish Pacifastacus leniusculus egg and spermatophore. Animal Reproduction Science. 2014a;149:335–344. doi: 10.1016/j.anireprosci.2014.07.024. PubMed DOI

Niksirat H, James P, Andersson L, Kouba A, Kozák P. Label-free protein quantification in freshly ejaculated versus post-mating spermatophores of the noble crayfish Astacus astacus. Journal of Proteomics. 2015b;123:70–77. doi: 10.1016/j.jprot.2015.04.004. PubMed DOI

Niksirat H, Kouba A. Subcellular localization of calcium deposits in the noble crayfish Astacus astacus spermatophore: implications for post-mating spermatophore hardening and spermatozoon maturation. Journal of Morphology. 2016;277:445–452. doi: 10.1002/jmor.20509. PubMed DOI

Niksirat H, Kouba A, Kozák P. Post-mating morphological changes in the spermatozoon and spermatophore wall of the crayfish Astacus leptodactylus: insight into a non-motile spermatozoon. Animal Reproduction Science. 2014b;149:325–334. doi: 10.1016/j.anireprosci.2014.07.017. PubMed DOI

Niksirat H, Kouba A, Kozák P. Ultrastructure of egg activation and cortical reaction in the noble crayfish Astacus astacus. Micron. 2015a;68:115–121. doi: 10.1016/j.micron.2014.09.010. PubMed DOI

Niksirat H, Kouba A, Pšenička M, Kuklina I, Kozák P. Ultrastructure of spermatozoa from three genera of crayfish Orconectes, Procambarus and Astacus (Decapoda: Astacoidea): new findings and comparisons. Zoologischer Anzeiger. 2013a;252:226–233. doi: 10.1016/j.jcz.2012.06.002. DOI

Niksirat H, Kouba A, Rodina M, Kozák P. Comparative ultrastructure of the spermatozoa of three crayfish species: Austropotamobius torrentium, Pacifastacus leniusculus, and Astacus astacus (Decapoda: Astacidae) Journal of Morphology. 2013b;274:750–758. doi: 10.1002/jmor.20132. PubMed DOI

Niksirat H, Vancová M, Andersson L, James P, Kouba A, Kozák P. Protein modification in the post-mating spermatophore of the signal crayfish Pacifastacus leniusculus: insight into the tyrosine phosphorylation in a non-motile spermatozoon. Animal Reproduction Science. 2016 doi: 10.1016/j.anireprosci.2016.07.009. In Press. PubMed DOI

Noro C, López-Greco LS, Buckup L. Gonad morphology and type of sexuality in Parastacus defossus Faxon 1898, a burrowing, intersexed crayfish from southern Brazil (Decapoda: Parastacidae) Acta Zoologica. 2008;89:59–67. doi: 10.1111/j.1463-6395.2007.00294.x. DOI

Pochon-Masson J. L’ Ultrastructure des spermatozoïdes vésiculaires chez les crustacés décapodes avant et au cours de leur dévagination expérimentale. II. Macroures. Discussion et conclusions’ Annales des Sciences Naturelles Zoologie Paris 12e serie. 1968;10:367–454.

Snedden WA. Determinants of male mating success in the temperate crayfish Orconectes Rusticus: Chela size and sperm competition. Behaviour. 1990;115:100–113. doi: 10.1163/156853990X00301. DOI

Tudge C. Spermatozoal morphology and its bearing on decapod phylogeny. In: Martin JW, Crandall KA, Felder DL, editors. Decapod crustacean phylogenetics. CRC Press. 2009. pp. 101–119.

Tudge CC, Scheltinga DM, Jamieson BG. Spermatozoal morphology in the “symmetrical” hermit crab, Pylocheles (Bathycheles) sp.(Crustacea, Decapoda, Anomura, Paguroidea, Pylochelidae) Zoosystema. 2001;23:117–130.

Vogt V. Functional anatomy. In: Holdich DM, editor. Biology of freshwater crayfish. Blackwell Science; Oxford: 2002. pp. 53–151.

Yasuzumi G, Kaye GI, Pappas GD, Yamamoto H, Tsubo I. Nuclear and cytoplasmic differentiation in developing sperm of the crayfish, Cambaroides japonicus. Zeitschrift für Zellforschung und mikroskopische Anatomie. 1961;53:141–158. doi: 10.1007/bf00339438. PubMed DOI

Yasuzumi G, Lee KJ. Spermatogenesis in animals as revealed by electron microscopy. Zeitschrift für Zellforschung und mikroskopische Anatomie. 1966;73:384–404. doi: 10.1007/bf00329018. PubMed DOI

Yazicioglu B, Linhartova Z, Niksirat H, Kozak P. First report of intersex in the signal crayfish Pacifastacus leniusculus (Dana, 1852) Crustaceana. 2014;87:1559–1566. doi: 10.1163/15685403-00003370. DOI