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Histomorphological investigation of the mature externa of Heterosaccus dollfusi (Crustacea, Rhizocephala)

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Abstract

The present investigation is the first in Egypt to give histomorphological data about Heterosaccus dollfusi, a rhizocephalan parasitic barnacle of the brachyuran crab Charybdis longicollis, collected from the eastern Mediterranean coast of Egypt at shallow depths (10–20 m). The structure of the mature externa and its male organs are essential for perception of both the taxonomy and reproductive biology of these specialized parasites. We use scanning electron microscopy and histological methods coupled with morphological description to investigate the anatomy of mature externa. The mature externa is distinguished by a visceral mass which comprises the ovary, paired colleteric glands, paired male receptacles and paired receptacle ducts. Attention is focused on the developmental stages of male organs and/or tracing of spermatozoa after settlement of male cypris implantation of the trichogon during fertilization process. For the first time, the lateral tube that connects the left male receptacle with the right, smaller receptacle was observed in sagittal section and illustrated in the diagrammatic figure of male organs. This tube is probably the generator of sperm ribbons. As well, the existence of the spermatozoa inside the lumen of this connecting tube may indicate their free movement between the two receptacles. Moreover, strips of sperm that drag from the sperm ribbon ball, and surround the developing ovules can also be seen in the mantle cavity.

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References

  • Alvarez F, Hines AH, Reaka-Kudla ML (1995) Effects of parasitism by the barnacle Loxothylacus panopaei (Gissler) (Cirripedia: Rhizocephala) on growth and survival of the host crab Rhithropanopeus harrisii (Gould) (Brachyura: Xanthidae). J Exp Mar Bio Ecol 192:221–232

    Article  Google Scholar 

  • Alvarez F, Bortolini J, Høeg JT (2010) Anatomy of virgin and mature externae of Loxothylacus texanus, parasitic on the dark blue crab Callinectes rathbunae (Crustacea: Cirripedia: Rhizocephala: Sacculinidae). J Morphol. https://doi.org/10.1002/jmor.10790

    Article  PubMed  Google Scholar 

  • Boschma H (1928) Rhizocephala. Dan Ingolf Exped 3(10):1–52

    Google Scholar 

  • Boschma H (1931) Die Rhizocephalen der Siboga. Expedition supplement. Siboga Expeditie 31bis:1–67

    Google Scholar 

  • Boschma H (1933) New species of Sacculinidae in the collection of the United States National Museum. Tijdschr Ned Dierkd Ver 3:219–241

    Google Scholar 

  • Boschma H (1957) Heterosaccus indicus, sp. nov., a rhizocephalan parasite of the crab Portunus pelagicus (L.). Ann Biol 2:1–20

    Google Scholar 

  • Boschma H (1960) A rhizocephalan parasite of the crab Charybdis hoplites (Wood-Mason). Crustaceana 1(58):67

    Google Scholar 

  • Boyko CB, Boxshall G (2018) World list of Rhizocephala. Heterosaccus Smith, 1906. Accessed through: world register of marine species at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=234070. Accessed 10 Aug 2018

  • Bresciani J, Høeg JT (2001) Comparative ultrastructure of the root system in Rhizocephalan barnacles (Crustacea: Cirripedia: Rhizocephala). J Morphol. https://doi.org/10.1002/jmor.1039

    Article  PubMed  Google Scholar 

  • Chan BKK (2004) First record of the parasitic barnacle Sacculina scabra Boschma 1931 (Crustacea: Cirripedia: Rhizocephala) infecting the shallow water swimming crab Charybdis truncata. Raffles B Zool 52(2):449–453

    Google Scholar 

  • Delage Y (1884) Evolution de la Sacculine (Sacculina carcini Thomps.), Crustace endoparasite de l’ordren ouveaud es Kentrogonides. Arch Zool Exp Gen 2(2):417–736

    Google Scholar 

  • Diechmann M, Høeg JT (1990) Boschmaella japonica, new species, a parasite on the barnacles Chthamalus challengeri and Balanus amphitrite amphitrite from Japan (Crustacea: Cirripedia: Rhizocephala: Chthamalophilidae). Acta Zool 71:173–175

    Article  Google Scholar 

  • Galil BS, Lützen J (1995) Biological observations on Heterosaccus dollfusi Boschma (Cirripedia: Rhizocephala), a parasite of Charybdis longicollis Leene (Decapoda: Brachyura), a lessepsian migrant to the Mediterranean. J Crustacean Biol 15:659–670

    Article  Google Scholar 

  • Galil BS, Lützen J (1998) Jeopardy: host and parasite lessepsian migrants from the Mediterranean coast of Israel. J Nat Hist 32:1549–1551

    Article  Google Scholar 

  • Glenner H, Hebsgaard MB (2006) Phylogeny and evolution of life history strategies of the parasitic barnacles (Crustacea, Cirripedia, Rhizocephala). Mol Phylogenet Evol. https://doi.org/10.1016/j.ympev.2006.06.004

    Article  PubMed  Google Scholar 

  • Glenner H, Høeg JT, O´Brien JJ, Sherman TD (2000) The invasive vermigon stage in the parasitic barnacles Loxothylacus texanus and L. panopaei (Sacculinidae): closing of the rhizocephalan life cycle. Mar Biol 136:249–257. https://doi.org/10.1007/s002270050683

    Article  Google Scholar 

  • Glenner H, Thomsen PF, Rybakov AV, Galil BS, Høeg JT (2008) The phylogeny of rhizocephalan parasites of the genus Heterosaccus using molecular and larval data (Cirripedia: Rhizocephala: Sacculinidae). Isr J Ecol Evol 54:223–238

    Article  Google Scholar 

  • Høeg JT (1982) The anatomy and development of the rhizocephalan barnacle Clistosaccus paguri to its host Pagurus bernhardus (L.). J Exp Mar Biol Ecol 58:87–125

    Article  Google Scholar 

  • Høeg JT (1985) Male cypris settlement in Clistosaccus paguri Lilljeborg (Crustacea: Cirripedia: Rhizocephala). J Exp Mar Biol Ecol 89:221–235

    Article  Google Scholar 

  • Høeg JT (1987) Male cypris metamorphosis and a new male larval form, the trichogon, in the parasitic barnacle Sacculina carcini (Crustacea: Cirripedia: Rhizocephala). Philos Trans R Soc Lond B Biol Sci 317:47–63

    Article  Google Scholar 

  • Høeg JT (1991) Functional and evolutionary aspects of the sexual system in the Rhizocephala (Crustacea: Thecostraca: Cirripedia). In: Bauer RT, Martin JW (eds) Crustacean sexual biology. Columbia University Press, New York, pp 208–227

    Chapter  Google Scholar 

  • Høeg JT (1992) Rhizocephala. In: Harrison FW, Humes AG (eds) Microscopic anatomy of invertebrates. Crustacea, vol 9. Wiley, New York, pp 313–345

    Google Scholar 

  • Høeg JT (1995) The biology and life cycle of the Rhizocephala (Cirripedia). J Mar Biol Assoc UK 75:517–550

    Article  Google Scholar 

  • Høeg JT, Lützen J (1995) Life cycle and reproduction in the Cirripedia Rhizocephala. Oceanogr Mar Biol An 33:427–485

    Google Scholar 

  • Høeg JT, Lützen J (1996) Rhizocephala. In: Forest J (ed) Traité de Zoologie, Crustacés, Généralités (suite) et Systématique, vol 7, vol 2. Masson et Cie, Paris, pp 541–568

    Google Scholar 

  • Høeg JT, Kapel CM, Thor P, Webster P (1990) The anatomy and sexual biology of Boschmaella japonica, an akentrogonid rhizocephalan parasite on barnacles from Japan (Crustacea: Cirripedia: Rhizocephala). Acta Zool 71:177–188

    Article  Google Scholar 

  • Høeg JT, Glenner H, Shields J (2005) Cirripedia Thoracica and Rhizocephala (barnacles). In: Rohde K (ed) Marine parasites. CABI Publishing, Wallingford, pp 154–165

    Google Scholar 

  • Holthuis LB (1961) Report on a collection of Crustacea Decapoda and Stomatopoda from Turkey and the Balkans. Zool Verh 47:1–67

    Google Scholar 

  • Ichikawa A, Yanagimachi R (1960) Studies on the sexual organization of the Rhizocephala. II. The reproductive function of the larval (cypris) males of Peltogaster and Sacculina. Annot Zool Jpn 33:42–56

    Google Scholar 

  • Innocenti G, Galil BS (2011) Live and let live: Invasive host, Charybdis longicollis (Decapoda: Brachyura: Portunidae), and invasive parasite, Heterosaccus dollfusi (Cirripedia: Rhizocephala: Sacculinidae). In: Galil BS et al (eds) In the wrong place—alien marine Crustaceans: distribution, biology and impacts, invading nature. Springer, Dordrecht, p 6

    Google Scholar 

  • Innocenti G, Galil BS, Yokeş MB, Diamant A, Goren M (2009) Here and there: a preliminary note on the prevalence of an alien Rhizocephalan parasite at the southern and northern limits of its introduced range. J Parasitol Res 95(6):1387–1390

    Article  Google Scholar 

  • Kruse I, Hare MP (2007) Genetic diversity and expanding nonindigenous range of the rhizocephalan Loxothylacus panopaei parasitizing mud crabs in the western North Atlantic. J Parasitol Res 93(3):575–582

    Article  CAS  Google Scholar 

  • Lange S (2002) The colleteric glands in Sacculinidae (Crustacea, Cirripedia, Rhizocephala): an ultrastructural study of ovisac secretion. Contrib Zool 70:229–242

    Article  Google Scholar 

  • Leene JE (1938) The Decapoda Brachyura of the Siboga Expedition. VII. Brachygnatha Portunidae Siboga-Expeditie 31:1–156

    Google Scholar 

  • Lützen J, Itani G, Jespersen Å, Hong J-S, Rees D, Glenner H (2016) On a new species of parasitic barnacle (Crustacea: Rhizocephala), Sacculina shiinoi sp. nov., parasitizing Japanese mud shrimps Upogebia spp. (Decapoda: Thalassinidea: Upogebiidae), including a description of a novel morphological structure in the Rhizocephala. Zool Sci 5:44. https://doi.org/10.2108/zs150112

    Article  Google Scholar 

  • Øksnebjerg B (2000) The Rhizocephala (Crustacea: Cirripedia) of the Mediterranean and Black Seas: taxonomy, biogeography, and ecology. Zool, Isr J. https://doi.org/10.1560/RCLC-NM2U-HV5L-6Q52

    Book  Google Scholar 

  • Øksnebjerg B, Enzenross R, Enzenross L (1997) First record of Rhizocephala (Crustcea: Cirripedia) from Turkish waters with notes on lessepsian migration. Stutt Beitr Naturkd Serie A (Biologie) 557:1–7

    Google Scholar 

  • Özcan T, Katağan T (2016) Prevalence of Heterosaccus dollfusi Boschma, 1960 (Rhizocephala: Sacculinidae) on Charybdis longicollis Leene, 1938 (Brachyura: Portunidae) from Iskenderun Bay, Turkey. J Black Sea Medit Environ 22:128–136

    Google Scholar 

  • Reinhard E (1942) The reproductive function of the complemental males of Peltogaster. J Morphol 70:389–402

    Article  Google Scholar 

  • Smith G (1906) Rhizocephala. Fauna und Flora des Golfes von Neapel 29:1–123

    Google Scholar 

  • Thompson JV (1836) Natural history and metamorphosis of an anomalous crustaceous parasite of Carcinus maenas, the Sacculina carcini. Entomol Mag 3:452–456

    Google Scholar 

  • WoRMS (2018). Rizocephala. http://www.marinespecies.org/aphia.php?p=taxadaetails&id=1109. Accessed 10 Aug 2018

  • Yanagimachi R, Fujimaki N (1967) Studies on the sexual organization of the Rhizocephala. IV. On the nature of the ‘‘testis” of Thompsonia. Annot Zool Jpn 40:98–104

    Google Scholar 

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Correspondence to Khaled M. Abdelsalam.

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This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This study did not involve endangered or protected species.

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Nour Eldeen, M.F., El Gamal, M.M., Abdelsalam, K.M. et al. Histomorphological investigation of the mature externa of Heterosaccus dollfusi (Crustacea, Rhizocephala). Zoomorphology 138, 463–473 (2019). https://doi.org/10.1007/s00435-019-00453-5

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